Direct Effects of HIV-1 Tat on Excitability and Survival of Primary Dorsal Root Ganglion Neurons: Possible Contribution to HIV-1-Associated Pain
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{"title"=>"Direct effects of HIV-1 tat on excitability and survival of primary dorsal root ganglion neurons: Possible contribution to HIV-1-associated pain", "type"=>"journal", "authors"=>[{"first_name"=>"Xianxun", "last_name"=>"Chi", "scopus_author_id"=>"51261048500"}, {"first_name"=>"Tohti", "last_name"=>"Amet", "scopus_author_id"=>"6506575505"}, {"first_name"=>"Daniel", "last_name"=>"Byrd", "scopus_author_id"=>"35298775900"}, {"first_name"=>"Kuei Hua", "last_name"=>"Chang", "scopus_author_id"=>"36463197000"}, {"first_name"=>"Kavita", "last_name"=>"Shah", "scopus_author_id"=>"7402959124"}, {"first_name"=>"Ningjie", "last_name"=>"Hu", "scopus_author_id"=>"26663452600"}, {"first_name"=>"Ayslinn", "last_name"=>"Grantham", "scopus_author_id"=>"51261121900"}, {"first_name"=>"Sishun", "last_name"=>"Hu", "scopus_author_id"=>"55475565900"}, {"first_name"=>"Jianhong", "last_name"=>"Duan", "scopus_author_id"=>"7202785837"}, {"first_name"=>"Feng", "last_name"=>"Tao", "scopus_author_id"=>"36875577300"}, {"first_name"=>"Grant", "last_name"=>"Nicol", "scopus_author_id"=>"7005589756"}, {"first_name"=>"Qigui", "last_name"=>"Yu", "scopus_author_id"=>"7402947490"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "pmid"=>"21912693", "pui"=>"362489445", "scopus"=>"2-s2.0-80052420493", "doi"=>"10.1371/journal.pone.0024412", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "sgr"=>"80052420493"}, "id"=>"45e215da-3938-30f3-b695-fd72011df9c0", "abstract"=>"The vast majority of people living with human immunodeficiency virus type 1 (HIV-1) have pain syndrome, which has a significant impact on their quality of life. The underlying causes of HIV-1-associated pain are not likely attributable to direct viral infection of the nervous system due to the lack of evidence of neuronal infection by HIV-1. However, HIV-1 proteins are possibly involved as they have been implicated in neuronal damage and death. The current study assesses the direct effects of HIV-1 Tat, one of potent neurotoxic viral proteins released from HIV-1-infected cells, on the excitability and survival of rat primary dorsal root ganglion (DRG) neurons. We demonstrated that HIV-1 Tat triggered rapid and sustained enhancement of the excitability of small-diameter rat primary DRG neurons, which was accompanied by marked reductions in the rheobase and resting membrane potential (RMP), and an increase in the resistance at threshold (R(Th)). Such Tat-induced DRG hyperexcitability may be a consequence of the inhibition of cyclin-dependent kinase 5 (Cdk5) activity. Tat rapidly inhibited Cdk5 kinase activity and mRNA production, and roscovitine, a well-known Cdk5 inhibitor, induced a very similar pattern of DRG hyperexcitability. Indeed, pre-application of Tat prevented roscovitine from having additional effects on the RMP and action potentials (APs) of DRGs. However, Tat-mediated actions on the rheobase and R(Th) were accelerated by roscovitine. These results suggest that Tat-mediated changes in DRG excitability are partly facilitated by Cdk5 inhibition. In addition, Cdk5 is most abundant in DRG neurons and participates in the regulation of pain signaling. We also demonstrated that HIV-1 Tat markedly induced apoptosis of primary DRG neurons after exposure for longer than 48 h. Together, this work indicates that HIV-1 proteins are capable of producing pain signaling through direct actions on excitability and survival of sensory neurons.", "link"=>"http://www.mendeley.com/research/direct-effects-hiv1-tat-excitability-survival-primary-dorsal-root-ganglion-neurons-possible-contribu", "reader_count"=>10, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Student > Doctoral Student"=>1, "Researcher"=>1, "Student > Ph. D. Student"=>2, "Student > Postgraduate"=>2, "Student > Master"=>2, "Student > Bachelor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Student > Doctoral Student"=>1, "Researcher"=>1, "Student > Ph. D. Student"=>2, "Student > Postgraduate"=>2, "Student > Master"=>2, "Student > Bachelor"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>1, "Agricultural and Biological Sciences"=>6, "Medicine and Dentistry"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>6}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"United States"=>2, "United Kingdom"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/740591"], "description"=>"<p>RMP: resting membrane potential; FT: firing threshold; R<sub>Th</sub>: resistance at threshold. Normalized rheobase: rheobase was normalized to the control. Normalized R<sub>Th</sub>: R<sub>Th</sub> was normalized to the control. Data are expressed as mean ± S.E.M. N = 15.</p><p>*<i>p</i><0.05;</p><p>**<i>p</i><0.01. Groups were compared with controls by Anova or Repeated Measures Anova.</p>", "links"=>[], "tags"=>["hiv-1", "tat", "parameters", "drg"], "article_id"=>410957, "categories"=>["Virology", "Molecular Biology", "Neuroscience", "Infectious Diseases"], "users"=>["Xianxun Chi", "Tohti Amet", "Daniel Byrd", "Kuei-Hua Chang", "Kavita Shah", "Ningjie Hu", "Ayslinn Grantham", "Sishun Hu", "Jianhong Duan", "Feng Tao", "Grant Nicol", "Qigui Yu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024412.t001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_effect_of_HIV_1_Tat_on_parameters_of_DRG_excitability_/410957", "title"=>"The effect of HIV-1 Tat on parameters of DRG excitability.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-20 15:14:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/740435"], "description"=>"<p>Parameters of DRG excitability including RMP, FT, Rheobase and R<sub>Th</sub> were compared between groups of Tat treatment alone versus Tat pretreatment followed by roscovitine exposure. The rheobase and R<sub>Th</sub> were normalized to their respective control values. Bars represent SEM on the mean. Asterisk indicates statistically significant (*<i>p</i><0.05; **<i>p</i><0.01) associations between the two groups at the same time point using Student T-test. Open bars: Tat alone, solid gray bars: Tat plus roscovitine. Ros: roscovitine, APs: action potentials, RMP: resting membrane potential; FT: firing threshold; and R<sub>Th</sub>: resistance at threshold.</p>", "links"=>[], "tags"=>["parameters", "drg", "excitability", "treatments", "tat", "verse"], "article_id"=>410792, "categories"=>["Virology", "Molecular Biology", "Neuroscience", "Infectious Diseases"], "users"=>["Xianxun Chi", "Tohti Amet", "Daniel Byrd", "Kuei-Hua Chang", "Kavita Shah", "Ningjie Hu", "Ayslinn Grantham", "Sishun Hu", "Jianhong Duan", "Feng Tao", "Grant Nicol", "Qigui Yu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024412.g005", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_parameters_of_DRG_excitability_between_treatments_of_Tat_alone_verse_Tat_then_roscovitine_/410792", "title"=>"Comparison of parameters of DRG excitability between treatments of Tat alone verse Tat then roscovitine.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 15:13:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/740360"], "description"=>"<p>Tat at 20 μM was focally applied to an individual DRG neuron to assess its actions over a 4 min time period, thereafter, the neuron was exposed to 10 μM roscovitine by external perfusion of the recording chamber. The whole-cell patch-clamp recordings were used to determine APs prior to Tat exposure (control), exposure to Tat or roscovitine or both. (A) A representative experiment of AP recording from one of five DRG neurons is shown. (B) Summary data from time points of Tat alone (n = 15) and Tat plus roscovitine co-exposure performed on all five DRG neurons are shown. Bars represent SEM on the mean. Ros: roscovitine, APs: action potentials.</p>", "links"=>[], "tags"=>["ap", "depolarization", "rmp", "affected"], "article_id"=>410726, "categories"=>["Virology", "Molecular Biology", "Neuroscience", "Infectious Diseases"], "users"=>["Xianxun Chi", "Tohti Amet", "Daniel Byrd", "Kuei-Hua Chang", "Kavita Shah", "Ningjie Hu", "Ayslinn Grantham", "Sishun Hu", "Jianhong Duan", "Feng Tao", "Grant Nicol", "Qigui Yu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024412.g004", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Tat_mediated_increase_of_AP_and_depolarization_of_RMP_were_not_affected_by_roscovitine_/410726", "title"=>"Tat-mediated increase of AP and depolarization of RMP were not affected by roscovitine.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 15:12:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/740282"], "description"=>"<p>Small-diameter rat primary DRG neurons were treated with Cdk5 inhibitor roscovitine (10 µM) or activator β-amyloid (10 µM), and then subjected to whole-cell patch-clamp recordings to determine action potentials (APs). (A) A representative experiment of AP recording from one of seven DRG neurons is shown. (B) Summary data from experiments performed on all seven DRG neurons are shown. Bars represent SEM on the mean. Comparisons were performed between PBS and roscovitine or β-amyloid according to time points of exposure using Anova or Repeated Measures Anova. Asterisk indicates statistically significant (<i>p</i><0.05) associations between PBS and roscovitine or β-amyloid according to time points of exposure. CN: control with PBS treatment, APs: action potentials.</p>", "links"=>[], "tags"=>["cdk5", "kinase", "enhanced", "excitability", "drg"], "article_id"=>410647, "categories"=>["Virology", "Molecular Biology", "Neuroscience", "Infectious Diseases"], "users"=>["Xianxun Chi", "Tohti Amet", "Daniel Byrd", "Kuei-Hua Chang", "Kavita Shah", "Ningjie Hu", "Ayslinn Grantham", "Sishun Hu", "Jianhong Duan", "Feng Tao", "Grant Nicol", "Qigui Yu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024412.g003", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Inhibition_of_Cdk5_kinase_activity_enhanced_the_excitability_of_DRG_neurons_/410647", "title"=>"Inhibition of Cdk5 kinase activity enhanced the excitability of DRG neurons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 15:12:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/740108"], "description"=>"<p>Small-diameter rat primary DRG neurons were treated with HIV-1 Tat, Gag or heat-inactivated Tat, and then subjected to whole-cell patch-clamp recordings to determine action potentials (APs). (A) A representative experiment of AP recording from one of fifteen DRG neurons is shown. The experiment was repeated at least two times. DRG neurons were exposed to 1 µM or 20 µM of Tat, 20 µM of Gag or 20 µM of heat-inactivated Tat, and the APs were recorded at 2 to 15 min of post-exposure to viral proteins. Treatment with PBS was used as a control to obtain the baseline of APs. (B) Summary data from experiments performed on all fifteen DRG neurons are shown. Bars represent SEM on the mean. Comparisons were performed between PBS and all conditions according to time points of exposure using Anova or Repeated Measures Anova. Asterisk indicates statistically significant (*<i>p</i><0.05) associations between PBS and Tat treatment according to time points of exposure. CN: control with PBS treatment, APs: action potentials.</p>", "links"=>[], "tags"=>["tat", "enhanced", "excitability", "small-diameter", "drg"], "article_id"=>410456, "categories"=>["Virology", "Molecular Biology", "Neuroscience", "Infectious Diseases"], "users"=>["Xianxun Chi", "Tohti Amet", "Daniel Byrd", "Kuei-Hua Chang", "Kavita Shah", "Ningjie Hu", "Ayslinn Grantham", "Sishun Hu", "Jianhong Duan", "Feng Tao", "Grant Nicol", "Qigui Yu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024412.g001", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HIV_1_Tat_enhanced_excitability_of_small_diameter_DRG_neurons_/410456", "title"=>"HIV-1 Tat enhanced excitability of small-diameter DRG neurons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 15:11:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/740192"], "description"=>"<p>(A) Cdk5 kinase activity in DRG neurons in response to exposure of HIV-1 Tat or Gag. Primary DRG neurons from rats were treated with 20 µM of HIV-1 Tat or Gag for various time intervals ranging from 15 min to 60 min, and were then subjected to Cdk5 kinase assays. Treatment with PBS was included to obtain the baseline of Cdk5 kinase activity. Open, solid gray, and solid black bars represent treatments of PBS, Tat, and Gag, respectively. Cdk5 kinase activity obtained from all conditions was normalized to PBS-treated controls. (B), (C) and (D) Direct effects of HIV-1 Tat and Gag on the regulation of Cdk5 mRNA and p35 mRNA levels in DRG neurons. DRG neurons were treated with 20 µM of HIV-1 Tat or Gag, or PBS for 4 h, and then subjected to analysis of Cdk5 or p35 mRNA production using (B) semi-quantitative RT-PCR and (C) and (D) real-time qPCR assays. Bars represent SD on the mean of three individual experiments. Asterisk indicates statistically significant (*<i>p</i><0.05; **<i>p</i><0.01) associations between PBS and Tat treatments.</p>", "links"=>[], "tags"=>["tat", "inhibited", "endogenous", "cdk5", "kinase", "mrna"], "article_id"=>410550, "categories"=>["Virology", "Molecular Biology", "Neuroscience", "Infectious Diseases"], "users"=>["Xianxun Chi", "Tohti Amet", "Daniel Byrd", "Kuei-Hua Chang", "Kavita Shah", "Ningjie Hu", "Ayslinn Grantham", "Sishun Hu", "Jianhong Duan", "Feng Tao", "Grant Nicol", "Qigui Yu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024412.g002", "stats"=>{"downloads"=>0, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HIV_1_Tat_inhibited_endogenous_Cdk5_kinase_activity_and_mRNA_production_/410550", "title"=>"HIV-1 Tat inhibited endogenous Cdk5 kinase activity and mRNA production.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 15:11:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/740644"], "description"=>"<p>RMP: resting membrane potential; FT: firing threshold; R<sub>Th</sub>: resistance at threshold. Normalized rheobase: rheobase was normalized to the control. Normalized R<sub>Th</sub>: R<sub>Th</sub> was normalized to the control. Data are expressed as mean ± S.E.M. N = 5.</p><p>*<i>p</i><0.05;</p><p>**<i>p</i><0.01. Groups were compared with controls by Anova or Repeated Measures Anova.</p>", "links"=>[], "tags"=>["parameters", "drg", "excitability", "treatments", "tat", "verse"], "article_id"=>411007, "categories"=>["Virology", "Molecular Biology", "Neuroscience", "Infectious Diseases"], "users"=>["Xianxun Chi", "Tohti Amet", "Daniel Byrd", "Kuei-Hua Chang", "Kavita Shah", "Ningjie Hu", "Ayslinn Grantham", "Sishun Hu", "Jianhong Duan", "Feng Tao", "Grant Nicol", "Qigui Yu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024412.t003", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_parameters_of_DRG_excitability_between_treatments_of_Tat_alone_verse_Tat_then_roscovitine_/411007", "title"=>"Comparison of parameters of DRG excitability between treatments of Tat alone verse Tat then roscovitine.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-20 15:14:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/740683"], "description"=>"<p>RMP: resting membrane potential; FT: firing threshold; R<sub>Th</sub>: resistance at threshold. Normalized rheobase: rheobase was normalized to the control. Normalized R<sub>Th</sub>: R<sub>Th</sub> was normalized to the control. Data are expressed as mean ± S.E.M. N = 7.</p><p>*<i>p</i><0.05;</p><p>**<i>p</i><0.01. Groups were compared with controls by Anova or Repeated Measures Anova.</p>", "links"=>[], "tags"=>["cdk5", "inhibitor", "activator", "parameters", "drg"], "article_id"=>411046, "categories"=>["Virology", "Molecular Biology", "Neuroscience", "Infectious Diseases"], "users"=>["Xianxun Chi", "Tohti Amet", "Daniel Byrd", "Kuei-Hua Chang", "Kavita Shah", "Ningjie Hu", "Ayslinn Grantham", "Sishun Hu", "Jianhong Duan", "Feng Tao", "Grant Nicol", "Qigui Yu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024412.t002", "stats"=>{"downloads"=>7, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_effect_of_Cdk5_inhibitor_or_activator_on_parameters_of_DRG_excitability_/411046", "title"=>"The effect of Cdk5 inhibitor or activator on parameters of DRG excitability.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-20 15:14:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/740519"], "description"=>"<p>Rat primary DRG neurons were exposed to 20 µM of HIV-1 Tat or Gag for 30 min to 72 h, and were then subjected to apoptosis analysis by Annexin-V staining and flow cytometric analysis. (A) DRG morphological changes in response to exposure of HIV-1 proteins for 48 h. (B) A representative annexin-v staining of DRG apoptosis in response to exposure of HIV-1 Tat or Gag for 48 h. Solid gray histogram represents a staining control without adding annexin-V<sup>FITC</sup>, whereas histograms with blue, green, and red lines represent annexin-V staining on DRG neurons treated with PBS, Gag, and Tat, respectively. (C) Summary data from three independent experiments of annexin-V staining on DRG neurons in response to exposure of HIV-1 Tat and Gag for 48 h or 72 h are shown. Bars represent SD on the mean of three individual experiments. Asterisk indicates statistically significant (<i>p</i><0.05) associations between PBS and Tat or Gag according to time points of exposure.</p>", "links"=>[], "tags"=>["neurons", "underwent", "apoptosis", "hiv-1"], "article_id"=>410879, "categories"=>["Virology", "Molecular Biology", "Neuroscience", "Infectious Diseases"], "users"=>["Xianxun Chi", "Tohti Amet", "Daniel Byrd", "Kuei-Hua Chang", "Kavita Shah", "Ningjie Hu", "Ayslinn Grantham", "Sishun Hu", "Jianhong Duan", "Feng Tao", "Grant Nicol", "Qigui Yu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024412.g006", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_DRG_neurons_underwent_apoptosis_in_response_to_chronic_exposure_of_HIV_1_Tat_/410879", "title"=>"DRG neurons underwent apoptosis in response to chronic exposure of HIV-1 Tat.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 15:13:41"}

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Relative Metric

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