Bioluminescent Imaging and Histopathologic Characterization of WEEV Neuroinvasion in Outbred CD-1 Mice
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{"title"=>"Bioluminescent Imaging and Histopathologic Characterization of WEEV Neuroinvasion in Outbred CD-1 Mice", "type"=>"journal", "authors"=>[{"first_name"=>"Aaron T.", "last_name"=>"Phillips", "scopus_author_id"=>"26423851000"}, {"first_name"=>"Charles B.", "last_name"=>"Stauft", "scopus_author_id"=>"55541157100"}, {"first_name"=>"Tawfik A.", "last_name"=>"Aboellail", "scopus_author_id"=>"26641864900"}, {"first_name"=>"Ann M.", "last_name"=>"Toth", "scopus_author_id"=>"15053907400"}, {"first_name"=>"Donald L.", "last_name"=>"Jarvis", "scopus_author_id"=>"7102858019"}, {"first_name"=>"Ann M.", "last_name"=>"Powers", "scopus_author_id"=>"7005770718"}, {"first_name"=>"Ken E.", "last_name"=>"Olson", "scopus_author_id"=>"7202013953"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"23301074", "sgr"=>"84871763475", "doi"=>"10.1371/journal.pone.0053462", "scopus"=>"2-s2.0-84871763475", "pui"=>"368034679", "isbn"=>"1932-6203 (Electronic)\\n1932-6203 (Linking)", "issn"=>"19326203"}, "id"=>"1d462bb5-5196-3b2c-a258-9656b932aa2a", "abstract"=>"Western equine encephalitis virus (WEEV; Alphavirus) is a mosquito-borne virus that can cause severe encephalitis in humans and equids. Previous studies have shown that intranasal infection of outbred CD-1 mice with the WEEV McMillan (McM) strain result in high mortality within 4 days of infection. Here in vivo and ex vivo bioluminescence (BLM) imaging was applied on mice intranasally infected with a recombinant McM virus expressing firefly luciferase (FLUC) to track viral neuroinvasion by FLUC detection and determine any correlation between BLM and viral titer. Immunological markers of disease (MCP-1 and IP-10) were measured and compared to wild type virus infection. Histopathology was guided by corresponding BLM images, and showed that neuroinvasion occurred primarily through cranial nerves, mainly in the olfactory tract. Olfactory bulb neurons were initially infected with subsequent spread of the infection into different regions of the brain. WEEV distribution was confirmed by immunohistochemistry as having marked neuronal infection but very few infected glial cells. Axons displayed infection patterns consistent with viral dissemination along the neuronal axis. The trigeminal nerve served as an additional route of neuroinvasion showing significant FLUC expression within the brainstem. The recombinant virus WEEV.McM.FLUC had attenuated replication kinetics and induced a weaker immunological response than WEEV.McM but produced comparable pathologies. Immunohistochemistry staining for FLUC and WEEV antigen showed that transgene expression was present in all areas of the CNS where virus was observed. BLM provides a quantifiable measure of alphaviral neural disease progression and a method for evaluating antiviral strategies.", "link"=>"http://www.mendeley.com/research/bioluminescent-imaging-histopathologic-characterization-weev-neuroinvasion-outbred-cd1-mice", "reader_count"=>20, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Researcher"=>5, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>1, "Student > Master"=>2, "Other"=>3, "Student > Bachelor"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Researcher"=>5, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>1, "Student > Master"=>2, "Other"=>3, "Student > Bachelor"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>1, "Agricultural and Biological Sciences"=>7, "Medicine and Dentistry"=>6, "Veterinary Science and Veterinary Medicine"=>2, "Chemistry"=>1, "Social Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>6}, "Chemistry"=>{"Chemistry"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>7}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}, "Unspecified"=>{"Unspecified"=>2}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>2}}, "reader_count_by_country"=>{"United Kingdom"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/515140"], "description"=>"<p>A) Cranial nerves including a branch of trigeminal nerve show neutrophilic perineuritis with a large glial nodule extending to the meninges of the overlying brain section (Bar = 200 µm). B) Close up of epineurium of cranial nerves infiltrated by neutrophils and lymphocytes (Bar = 100 µm). C & D) Strong immunoreactivity (anti-FLUC) of maxillary nerve including Schwann cells. Note strong and diffuse immunoreactivity of olfactory neuropeithelium, variable staining of surrounding skeletal muscles and bone marrow elements (Bar = 100 µm). E) Trigeminal ganglion IHC positivity (Bar = 100 µm). F) Trigeminal positivity is associated with immunoreactivity of the overlying meninges and brain tissue (Bar = 100 µm). G) Brainstem demyelinating lesion (potential consequence of trigeminal invasion) (Bar = 400 µm). H) IHC positivity (anti-FLUC) in the brain stem with interneuronal spread and rare immunoreactivity of glial cells (astrocytes) (Bar = 100 µm). All IHC images within this figure are from anti-FLUC staining. Comparison images using anti-WEEV staining may be found in the supplemental information.</p>", "links"=>[], "tags"=>["trigeminal"], "article_id"=>185636, "categories"=>["Virology", "Neuroscience"], "users"=>["Aaron T. Phillips", "Charles B. Stauft", "Tawfik A. Aboellail", "Ann M. Toth", "Donald L. Jarvis", "Ann M. Powers", "Ken E. Olson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0053462.g005", "stats"=>{"downloads"=>1, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Neuroinvasion_from_trigeminal_nerve_/185636", "title"=>"Neuroinvasion from trigeminal nerve.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-01-02 01:33:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/514398"], "description"=>"<p>AON: anterior olfactory nucleus, BF: basal forebrain, CC: cerebral cortex (isocortex), CP: caudate putamen, F: fornix, HIP: hippocampus, OB: olfactory bulb, VS: ventral striatum. Progress of infection with WEEV after intranasal inoculation (A–D). Whole heads were bisected along sagittal midline and imaged at 24 hpi (A), 48 hpi (B), 60 hpi (C) and 72 hpi (D). Luciferase activity pattern is consistent with dissemination along olfactory pathways. Regions consistent with initial infection of the nasal turbinates show pronounced FLUC activity at 24 hpi. However, nasal turbinate BLM activity is exceeded by signal from areas consistent with infection proceeding through olfactory information processing within the CNS, including the lateral olfactory tract, anterior olfactory nucleus, basal ganglia, thalamus, and cerebrum. Immunological markers of disease (MCP-1 and IP-10), resulting from WEEV.MCM.FLUC, are strongly induced and comparable to WEEV.McM at 3 d.p.i. (E–F).</p>", "links"=>[], "tags"=>["depiction", "anatomical", "medial", "sagittal"], "article_id"=>184886, "categories"=>["Virology", "Neuroscience"], "users"=>["Aaron T. Phillips", "Charles B. Stauft", "Tawfik A. Aboellail", "Ann M. Toth", "Donald L. Jarvis", "Ann M. Powers", "Ken E. Olson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0053462.g002", "stats"=>{"downloads"=>8, "page_views"=>314, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Schematic_depiction_of_anatomical_organization_of_mouse_brain_in_medial_sagittal_view_/184886", "title"=>"Schematic depiction of anatomical organization of mouse brain in medial sagittal view.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-01-02 01:21:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/514238"], "description"=>"<p>A: 24 hpi B: 48 hpi C: 72 hpi D: Survival analysis of WEEV.McM.FLUC and wild-type virus (WEEV.McM) from subcutaneous and intranasal virus challenge experiments. Note uniform lethality resulting from intranasal exposure by WEEV.McM.FLUC. E: FLUC activity was quantitatively measured in each animal at 1, 2, and 3 d.p.i. time points. Results from BLM analysis demonstrate robust FLUC activity as infection progressed with the greatest increase observed between days 2 and 3 post-infection. F: Brains of animals infected with WEEV.McM attain a higher viral titer more rapidly when compared with WEEV.McM.FLUC. WEEV.McM.FLUC titers approach that of McM by 72 h.p.i. G: Regression analysis of viral titer versus FLUC activity. Linear regression line appears curved due to log10 scaling of axis as required to clearly depict all data points (R<sup>2</sup> = 0.9807).</p>", "links"=>[], "tags"=>["blm", "imaging"], "article_id"=>184728, "categories"=>["Virology", "Neuroscience"], "users"=>["Aaron T. Phillips", "Charles B. Stauft", "Tawfik A. Aboellail", "Ann M. Toth", "Donald L. Jarvis", "Ann M. Powers", "Ken E. Olson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0053462.g001", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_In_vivo_BLM_imaging_of_infection_progress_using_WEEV_McM_FLUC_/184728", "title"=>"<i>In vivo</i> BLM imaging of infection progress using WEEV.McM.FLUC.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-01-02 01:18:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/515334"], "description"=>"<p>A) Average radiance in vaccinated, untreated, and uninfected mice at 48 hpi. Treated animals show significantly reduced luciferase activity (<i>p</i><0.01) compared to untreated animals. Error bars indicate standard deviation. B) Corresponding images used for the quantitative analysis. Scale was normalized for all images and is shown on the left-hand side. Images presented are from 48 hours post intranasal challenge with WEEV.McM.FLUC.</p>", "links"=>[], "tags"=>["imaging", "liposome-antigen-nucleic", "acid-complex", "vaccination"], "article_id"=>185820, "categories"=>["Virology", "Neuroscience"], "users"=>["Aaron T. Phillips", "Charles B. Stauft", "Tawfik A. Aboellail", "Ann M. Toth", "Donald L. Jarvis", "Ann M. Powers", "Ken E. Olson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0053462.g006", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_In_vivo_imaging_assessment_of_liposome_antigen_nucleic_acid_complex_vaccination_strategy_/185820", "title"=>"<i>In vivo</i> imaging assessment of liposome-antigen-nucleic acid-complex vaccination strategy.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-01-02 01:37:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/514861"], "description"=>"<p>A) Expanded view of the olfactory bulb showing progression of virus into caudal regions of the brain with multifocal necrosis and secondary demyelination (arrows) (Bar = 1000 µm). B) Multifocal demyelination and positive immunoreactivity in the anterior olfactory nucleus (AON), ventral striatum (VS), basal forebrain (BF) thalamus, hypothalamus, midbrain, hippocampus (HIP), and cerebral cortex (CC). Fornix (F) and optic tract (circled in blue) do not show any immunoreactivity (Bar = 1000 µm). C) Neuronal immunoreactivity in caudal olfactory bulb that shows multifocal demyelinating lesions (Bar = 100 µm). D) Multifocal immunoreactivity in caudal olfactory bulb and anterior olfactory nucleus (Bar = 200 µm). E) Strong immunoreactivity in hippocampus (Bar = 100 µm). F) Hippocampal H&E showing focal loss of pyramidal neurons with mild gliosis (Bar = 100 µm). G) Multifocal areas of necrosis and demylelination in the cerebral cortex (Bar = 200 µm). H) Strong immunoreactivity in cerebral neurons and their dendrites revealing interneuronal spread (Bar = 100 µm). All IHC images within this figure are from anti-FLUC staining. Comparison images using anti-WEEV staining may be found in the supplemental information.</p>", "links"=>[], "tags"=>["dissemination", "72"], "article_id"=>185359, "categories"=>["Virology", "Neuroscience"], "users"=>["Aaron T. Phillips", "Charles B. Stauft", "Tawfik A. Aboellail", "Ann M. Toth", "Donald L. Jarvis", "Ann M. Powers", "Ken E. Olson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0053462.g004", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Later_stage_dissemination_throughout_the_brain_72_hpi_/185359", "title"=>"Later stage dissemination throughout the brain 72 hpi.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-01-02 01:29:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/514622"], "description"=>"<p>A) Focal erosion/necrosis of the olfactory mucosa with deciliation of the flanking epithelium and neutrophil infiltration into the mucosa and submucosa (Bar = 100 µm). B) IHC positive staining for FLUC is highlighted in a few neuropeithelial cells subjacent to a focal loss of olfactory mucosa (Bar = 200 µm). <b>II- Neuroinvasion from olfactory nerve 48–72 hpi.</b> C) Terminal end of olfactory nerve shows a digestion chamber (arrow) with occasional lymphocytes infiltrating vacuolated branches (Bar = 100 µm). D) Early immunoreactivity (anti-FLUC) in the main olfactory bulb involving scattered neurons in the external plexiform and granular layers (Bar = 100 µm). E) Sagittal section H&E showing the connection between olfactory nerve (ON) and main olfactory bulb layers affected by multifocal necrotizing lesions with associated status spongiosis and infiltration of neutrophils. Glom = glomerular layer; EPI = external plexiform layer; IPL = internal plexiform layer; and ONL = olfactory nerve layer at the ventrum of the olfactory bulb (Bar = 400 µm). F) Neuropil of the olfactory nerve layer shows a large vacuolar lesion (demyelination) with individual neuronal necrosis and infiltration of small numbers of neutrophils (Bar = 100 µm). G) Perivascular cuffs and multifocal gliosis in the glomerular layer 72 hpi (Bar = 200 µm). H) Close-up view of the congested glomerular vessels with pleocellular perivascular cuffs comprising moderate numbers of neutrophils, lymphocytes and glial cells (Bar = 100 µm).</p>", "links"=>[], "tags"=>["extraneural", "lesions", "24"], "article_id"=>185116, "categories"=>["Virology", "Neuroscience"], "users"=>["Aaron T. Phillips", "Charles B. Stauft", "Tawfik A. Aboellail", "Ann M. Toth", "Donald L. Jarvis", "Ann M. Powers", "Ken E. Olson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0053462.g003", "stats"=>{"downloads"=>3, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_I_Extraneural_lesions_24_hpi_/185116", "title"=>"I. Extraneural lesions 24 hpi.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-01-02 01:25:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/280197", "https://ndownloader.figshare.com/files/280232", "https://ndownloader.figshare.com/files/280368", "https://ndownloader.figshare.com/files/280432", "https://ndownloader.figshare.com/files/280475"], "description"=>"<div><p>Western equine encephalitis virus (WEEV; <em>Alphavirus</em>) is a mosquito-borne virus that can cause severe encephalitis in humans and equids. Previous studies have shown that intranasal infection of outbred CD-1 mice with the WEEV McMillan (McM) strain result in high mortality within 4 days of infection. Here <em>in vivo</em> and <em>ex vivo</em> bioluminescence (BLM) imaging was applied on mice intranasally infected with a recombinant McM virus expressing firefly luciferase (FLUC) to track viral neuroinvasion by FLUC detection and determine any correlation between BLM and viral titer. Immunological markers of disease (MCP-1 and IP-10) were measured and compared to wild type virus infection. Histopathology was guided by corresponding BLM images, and showed that neuroinvasion occurred primarily through cranial nerves, mainly in the olfactory tract. Olfactory bulb neurons were initially infected with subsequent spread of the infection into different regions of the brain. WEEV distribution was confirmed by immunohistochemistry as having marked neuronal infection but very few infected glial cells. Axons displayed infection patterns consistent with viral dissemination along the neuronal axis. The trigeminal nerve served as an additional route of neuroinvasion showing significant FLUC expression within the brainstem. The recombinant virus WEEV.McM.FLUC had attenuated replication kinetics and induced a weaker immunological response than WEEV.McM but produced comparable pathologies. Immunohistochemistry staining for FLUC and WEEV antigen showed that transgene expression was present in all areas of the CNS where virus was observed. BLM provides a quantifiable measure of alphaviral neural disease progression and a method for evaluating antiviral strategies.</p> </div>", "links"=>[], "tags"=>["bioluminescent", "imaging", "histopathologic", "characterization", "weev", "neuroinvasion", "outbred", "cd-1", "mice"], "article_id"=>115247, "categories"=>["Neuroscience", "Cancer"], "users"=>["Aaron T. Phillips", "Charles B. Stauft", "Tawfik A. Aboellail", "Ann M. Toth", "Donald L. Jarvis", "Ann M. Powers", "Ken E. Olson"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0053462.s001", "https://dx.doi.org/10.1371/journal.pone.0053462.s002", "https://dx.doi.org/10.1371/journal.pone.0053462.s003", "https://dx.doi.org/10.1371/journal.pone.0053462.s004", "https://dx.doi.org/10.1371/journal.pone.0053462.s005"], "stats"=>{"downloads"=>9, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Bioluminescent_Imaging_and_Histopathologic_Characterization_of_WEEV_Neuroinvasion_in_Outbred_CD_1_Mice__/115247", "title"=>"Bioluminescent Imaging and Histopathologic Characterization of WEEV Neuroinvasion in Outbred CD-1 Mice", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-01-02 01:27:27"}

PMC Usage Stats | Further Information

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Relative Metric

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