Dengue Virus Type 2 (DENV2)-Induced Oxidative Responses in Monocytes from Glucose-6-Phosphate Dehydrogenase (G6PD)-Deficient and G6PD Normal Subjects
Identifieur interne : 000417 ( Pmc/Checkpoint ); précédent : 000416; suivant : 000418Dengue Virus Type 2 (DENV2)-Induced Oxidative Responses in Monocytes from Glucose-6-Phosphate Dehydrogenase (G6PD)-Deficient and G6PD Normal Subjects
Auteurs : Abdullah Ahmed Al-Alimi [Malaisie] ; Syed A. Ali [Malaisie] ; Faisal Muti Al-Hassan [Malaisie] ; Fauziah Mohd Idris [Malaisie] ; Sin-Yeang Teow [Malaisie] ; Narazah Mohd Yusoff [Malaisie]Source :
- PLoS Neglected Tropical Diseases [ 1935-2727 ] ; 2014.
Abstract
Dengue virus is endemic in peninsular Malaysia. The clinical manifestations vary depending on the incubation period of the virus as well as the immunity of the patients. Glucose-6-phosphate dehydrogenase (G6PD) deficiency is prevalent in Malaysia where the incidence is 3.2%. It has been noted that some G6PD-deficient individuals suffer from more severe clinical presentation of dengue infection. In this study, we aim to investigate the oxidative responses of DENV2-infected monocytes from G6PD-deficient individuals.
Monocytes from G6PD-deficient individuals were infected with DENV2 and infection rate, levels of oxidative species, nitric oxide (NO), superoxide anions (O2−), and oxidative stress were determined and compared with normal controls.
Monocytes from G6PD-deficient individuals exhibited significantly higher infection rates compared to normal controls. In an effort to explain the reason for this enhanced susceptibility, we investigated the production of NO and O2− in the monocytes of individuals with G6PD deficiency compared with normal controls. We found that levels of NO and O2− were significantly lower in the DENV-infected monocytes from G6PD-deficient individuals compared with normal controls. Furthermore, the overall oxidative stress in DENV-infected monocytes from G6PD-deficient individuals was significantly higher when compared to normal controls. Correlation studies between DENV-infected cells and oxidative state of monocytes further confirmed these findings.
Altered redox state of DENV-infected monocytes from G6PD-deficient individuals appears to augment viral replication in these cells. DENV-infected G6PD-deficient individuals may contain higher viral titers, which may be significant in enhanced virus transmission. Furthermore, granulocyte dysfunction and higher viral loads in G6PD-deificient individuals may result in severe form of dengue infection.
Url:
DOI: 10.1371/journal.pntd.0002711
PubMed: 24625456
PubMed Central: 3953068
Affiliations:
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Dengue Virus Type 2 (DENV2)-Induced Oxidative Responses in Monocytes from Glucose-6-Phosphate Dehydrogenase (G6PD)-Deficient and G6PD Normal Subjects</title><author><name sortKey="Al Alimi, Abdullah Ahmed" sort="Al Alimi, Abdullah Ahmed" uniqKey="Al Alimi A" first="Abdullah Ahmed" last="Al-Alimi">Abdullah Ahmed Al-Alimi</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Advanced Medical and Dental Institute, Universiti Sains Malaysia, Bertam, Penang, Malaysia</addr-line></nlm:aff><country xml:lang="fr">Malaisie</country><wicri:regionArea>Advanced Medical and Dental Institute, Universiti Sains Malaysia, Bertam, Penang</wicri:regionArea><wicri:noRegion>Penang</wicri:noRegion></affiliation></author><author><name sortKey="Ali, Syed A" sort="Ali, Syed A" uniqKey="Ali S" first="Syed A." last="Ali">Syed A. Ali</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Advanced Medical and Dental Institute, Universiti Sains Malaysia, Bertam, Penang, Malaysia</addr-line></nlm:aff><country xml:lang="fr">Malaisie</country><wicri:regionArea>Advanced Medical and Dental Institute, Universiti Sains Malaysia, Bertam, Penang</wicri:regionArea><wicri:noRegion>Penang</wicri:noRegion></affiliation></author><author><name sortKey="Al Hassan, Faisal Muti" sort="Al Hassan, Faisal Muti" uniqKey="Al Hassan F" first="Faisal Muti" last="Al-Hassan">Faisal Muti Al-Hassan</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Advanced Medical and Dental Institute, Universiti Sains Malaysia, Bertam, Penang, Malaysia</addr-line></nlm:aff><country xml:lang="fr">Malaisie</country><wicri:regionArea>Advanced Medical and Dental Institute, Universiti Sains Malaysia, Bertam, Penang</wicri:regionArea><wicri:noRegion>Penang</wicri:noRegion></affiliation></author><author><name sortKey="Idris, Fauziah Mohd" sort="Idris, Fauziah Mohd" uniqKey="Idris F" first="Fauziah Mohd" last="Idris">Fauziah Mohd Idris</name><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Department of Microbiology, School of Medical Sciences, Universiti Sains Malaysia, Kubang Kerian, Kelantan, Malaysia</addr-line></nlm:aff><country xml:lang="fr">Malaisie</country><wicri:regionArea>Department of Microbiology, School of Medical Sciences, Universiti Sains Malaysia, Kubang Kerian, Kelantan</wicri:regionArea><wicri:noRegion>Kelantan</wicri:noRegion></affiliation></author><author><name sortKey="Teow, Sin Yeang" sort="Teow, Sin Yeang" uniqKey="Teow S" first="Sin-Yeang" last="Teow">Sin-Yeang Teow</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Advanced Medical and Dental Institute, Universiti Sains Malaysia, Bertam, Penang, Malaysia</addr-line></nlm:aff><country xml:lang="fr">Malaisie</country><wicri:regionArea>Advanced Medical and Dental Institute, Universiti Sains Malaysia, Bertam, Penang</wicri:regionArea><wicri:noRegion>Penang</wicri:noRegion></affiliation></author><author><name sortKey="Mohd Yusoff, Narazah" sort="Mohd Yusoff, Narazah" uniqKey="Mohd Yusoff N" first="Narazah" last="Mohd Yusoff">Narazah Mohd Yusoff</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Advanced Medical and Dental Institute, Universiti Sains Malaysia, Bertam, Penang, Malaysia</addr-line></nlm:aff><country xml:lang="fr">Malaisie</country><wicri:regionArea>Advanced Medical and Dental Institute, Universiti Sains Malaysia, Bertam, Penang</wicri:regionArea><wicri:noRegion>Penang</wicri:noRegion></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">24625456</idno><idno type="pmc">3953068</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3953068</idno><idno type="RBID">PMC:3953068</idno><idno type="doi">10.1371/journal.pntd.0002711</idno><date when="2014">2014</date><idno type="wicri:Area/Pmc/Corpus">000670</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000670</idno><idno type="wicri:Area/Pmc/Curation">000670</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000670</idno><idno type="wicri:Area/Pmc/Checkpoint">000417</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000417</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Dengue Virus Type 2 (DENV2)-Induced Oxidative Responses in Monocytes from Glucose-6-Phosphate Dehydrogenase (G6PD)-Deficient and G6PD Normal Subjects</title><author><name sortKey="Al Alimi, Abdullah Ahmed" sort="Al Alimi, Abdullah Ahmed" uniqKey="Al Alimi A" first="Abdullah Ahmed" last="Al-Alimi">Abdullah Ahmed Al-Alimi</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Advanced Medical and Dental Institute, Universiti Sains Malaysia, Bertam, Penang, Malaysia</addr-line></nlm:aff><country xml:lang="fr">Malaisie</country><wicri:regionArea>Advanced Medical and Dental Institute, Universiti Sains Malaysia, Bertam, Penang</wicri:regionArea><wicri:noRegion>Penang</wicri:noRegion></affiliation></author><author><name sortKey="Ali, Syed A" sort="Ali, Syed A" uniqKey="Ali S" first="Syed A." last="Ali">Syed A. Ali</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Advanced Medical and Dental Institute, Universiti Sains Malaysia, Bertam, Penang, Malaysia</addr-line></nlm:aff><country xml:lang="fr">Malaisie</country><wicri:regionArea>Advanced Medical and Dental Institute, Universiti Sains Malaysia, Bertam, Penang</wicri:regionArea><wicri:noRegion>Penang</wicri:noRegion></affiliation></author><author><name sortKey="Al Hassan, Faisal Muti" sort="Al Hassan, Faisal Muti" uniqKey="Al Hassan F" first="Faisal Muti" last="Al-Hassan">Faisal Muti Al-Hassan</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Advanced Medical and Dental Institute, Universiti Sains Malaysia, Bertam, Penang, Malaysia</addr-line></nlm:aff><country xml:lang="fr">Malaisie</country><wicri:regionArea>Advanced Medical and Dental Institute, Universiti Sains Malaysia, Bertam, Penang</wicri:regionArea><wicri:noRegion>Penang</wicri:noRegion></affiliation></author><author><name sortKey="Idris, Fauziah Mohd" sort="Idris, Fauziah Mohd" uniqKey="Idris F" first="Fauziah Mohd" last="Idris">Fauziah Mohd Idris</name><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Department of Microbiology, School of Medical Sciences, Universiti Sains Malaysia, Kubang Kerian, Kelantan, Malaysia</addr-line></nlm:aff><country xml:lang="fr">Malaisie</country><wicri:regionArea>Department of Microbiology, School of Medical Sciences, Universiti Sains Malaysia, Kubang Kerian, Kelantan</wicri:regionArea><wicri:noRegion>Kelantan</wicri:noRegion></affiliation></author><author><name sortKey="Teow, Sin Yeang" sort="Teow, Sin Yeang" uniqKey="Teow S" first="Sin-Yeang" last="Teow">Sin-Yeang Teow</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Advanced Medical and Dental Institute, Universiti Sains Malaysia, Bertam, Penang, Malaysia</addr-line></nlm:aff><country xml:lang="fr">Malaisie</country><wicri:regionArea>Advanced Medical and Dental Institute, Universiti Sains Malaysia, Bertam, Penang</wicri:regionArea><wicri:noRegion>Penang</wicri:noRegion></affiliation></author><author><name sortKey="Mohd Yusoff, Narazah" sort="Mohd Yusoff, Narazah" uniqKey="Mohd Yusoff N" first="Narazah" last="Mohd Yusoff">Narazah Mohd Yusoff</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Advanced Medical and Dental Institute, Universiti Sains Malaysia, Bertam, Penang, Malaysia</addr-line></nlm:aff><country xml:lang="fr">Malaisie</country><wicri:regionArea>Advanced Medical and Dental Institute, Universiti Sains Malaysia, Bertam, Penang</wicri:regionArea><wicri:noRegion>Penang</wicri:noRegion></affiliation></author></analytic><series><title level="j">PLoS Neglected Tropical Diseases</title><idno type="ISSN">1935-2727</idno><idno type="eISSN">1935-2735</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p>Dengue virus is endemic in peninsular Malaysia. The clinical manifestations vary depending on the incubation period of the virus as well as the immunity of the patients. Glucose-6-phosphate dehydrogenase (G6PD) deficiency is prevalent in Malaysia where the incidence is 3.2%. It has been noted that some G6PD-deficient individuals suffer from more severe clinical presentation of dengue infection. In this study, we aim to investigate the oxidative responses of DENV2-infected monocytes from G6PD-deficient individuals.</p></sec><sec><title>Methodology</title><p>Monocytes from G6PD-deficient individuals were infected with DENV2 and infection rate, levels of oxidative species, nitric oxide (NO), superoxide anions (O<sub>2</sub><sup>−</sup>), and oxidative stress were determined and compared with normal controls.</p></sec><sec><title>Principal Findings</title><p>Monocytes from G6PD-deficient individuals exhibited significantly higher infection rates compared to normal controls. In an effort to explain the reason for this enhanced susceptibility, we investigated the production of NO and O<sub>2</sub><sup>−</sup> in the monocytes of individuals with G6PD deficiency compared with normal controls. We found that levels of NO and O<sub>2</sub><sup>−</sup> were significantly lower in the DENV-infected monocytes from G6PD-deficient individuals compared with normal controls. Furthermore, the overall oxidative stress in DENV-infected monocytes from G6PD-deficient individuals was significantly higher when compared to normal controls. Correlation studies between DENV-infected cells and oxidative state of monocytes further confirmed these findings.</p></sec><sec><title>Conclusions/Significance</title><p>Altered redox state of DENV-infected monocytes from G6PD-deficient individuals appears to augment viral replication in these cells. DENV-infected G6PD-deficient individuals may contain higher viral titers, which may be significant in enhanced virus transmission. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS Negl Trop Dis</journal-id><journal-id journal-id-type="iso-abbrev">PLoS Negl Trop Dis</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plosntds</journal-id><journal-title-group><journal-title>PLoS Neglected Tropical Diseases</journal-title></journal-title-group><issn pub-type="ppub">1935-2727</issn><issn pub-type="epub">1935-2735</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">24625456</article-id><article-id pub-id-type="pmc">3953068</article-id><article-id pub-id-type="publisher-id">PNTD-D-12-01358</article-id><article-id pub-id-type="doi">10.1371/journal.pntd.0002711</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v2"><subject>Biology</subject><subj-group><subject>Genetics</subject></subj-group><subj-group><subject>Immunology</subject></subj-group><subj-group><subject>Microbiology</subject></subj-group><subj-group><subject>Molecular Cell Biology</subject></subj-group></subj-group></article-categories><title-group><article-title>Dengue Virus Type 2 (DENV2)-Induced Oxidative Responses in Monocytes from Glucose-6-Phosphate Dehydrogenase (G6PD)-Deficient and G6PD Normal Subjects</article-title><alt-title alt-title-type="running-head">G6PD Deficiency Ameliorates DENV2 Infection</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Al-alimi</surname><given-names>Abdullah Ahmed</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Ali</surname><given-names>Syed A.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Al-Hassan</surname><given-names>Faisal Muti</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Idris</surname><given-names>Fauziah Mohd</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Teow</surname><given-names>Sin-Yeang</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Mohd Yusoff</surname><given-names>Narazah</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="corresp" rid="cor1"><sup>*</sup></xref></contrib></contrib-group><aff id="aff1"><label>1</label><addr-line>Advanced Medical and Dental Institute, Universiti Sains Malaysia, Bertam, Penang, Malaysia</addr-line></aff><aff id="aff2"><label>2</label><addr-line>Department of Microbiology, School of Medical Sciences, Universiti Sains Malaysia, Kubang Kerian, Kelantan, Malaysia</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Guzman</surname><given-names>Maria G.</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>Tropical Medicine Institute Pedro Kourí, Cuba</addr-line></aff><author-notes><corresp id="cor1">* E-mail: <email>Narazah@amdi.usm.edu.my</email></corresp><fn fn-type="COI-statement"><p>The authors have declared that no competing interests exist.</p></fn><fn fn-type="con"><p>Conceived and designed the experiments: SAA FMAH NMY. Performed the experiments: AAAa SAA SYT. Analyzed the data: SAA SYT. Contributed reagents/materials/analysis tools: FMI NMY. Wrote the paper: AAAa SAA.</p></fn></author-notes><pub-date pub-type="collection"><month>3</month><year>2014</year></pub-date><pub-date pub-type="epub"><day>13</day><month>3</month><year>2014</year></pub-date><volume>8</volume><issue>3</issue><elocation-id>e2711</elocation-id><history><date date-type="received"><day>22</day><month>10</month><year>2012</year></date><date date-type="accepted"><day>9</day><month>1</month><year>2014</year></date></history><permissions><copyright-statement>© 2014 Al-alimi et al</copyright-statement><copyright-year>2014</copyright-year><copyright-holder>Al-alimi et al</copyright-holder><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.</license-p></license></permissions><abstract><sec><title>Background</title><p>Dengue virus is endemic in peninsular Malaysia. The clinical manifestations vary depending on the incubation period of the virus as well as the immunity of the patients. Glucose-6-phosphate dehydrogenase (G6PD) deficiency is prevalent in Malaysia where the incidence is 3.2%. It has been noted that some G6PD-deficient individuals suffer from more severe clinical presentation of dengue infection. In this study, we aim to investigate the oxidative responses of DENV2-infected monocytes from G6PD-deficient individuals.</p></sec><sec><title>Methodology</title><p>Monocytes from G6PD-deficient individuals were infected with DENV2 and infection rate, levels of oxidative species, nitric oxide (NO), superoxide anions (O<sub>2</sub><sup>−</sup>), and oxidative stress were determined and compared with normal controls.</p></sec><sec><title>Principal Findings</title><p>Monocytes from G6PD-deficient individuals exhibited significantly higher infection rates compared to normal controls. In an effort to explain the reason for this enhanced susceptibility, we investigated the production of NO and O<sub>2</sub><sup>−</sup> in the monocytes of individuals with G6PD deficiency compared with normal controls. We found that levels of NO and O<sub>2</sub><sup>−</sup> were significantly lower in the DENV-infected monocytes from G6PD-deficient individuals compared with normal controls. Furthermore, the overall oxidative stress in DENV-infected monocytes from G6PD-deficient individuals was significantly higher when compared to normal controls. Correlation studies between DENV-infected cells and oxidative state of monocytes further confirmed these findings.</p></sec><sec><title>Conclusions/Significance</title><p>Altered redox state of DENV-infected monocytes from G6PD-deficient individuals appears to augment viral replication in these cells. DENV-infected G6PD-deficient individuals may contain higher viral titers, which may be significant in enhanced virus transmission. Furthermore, granulocyte dysfunction and higher viral loads in G6PD-deificient individuals may result in severe form of dengue infection.</p></sec></abstract><abstract abstract-type="summary"><title>Author Summary</title><p>An estimated 50 to 100 million cases of dengue fever occur each year worldwide. Among these, there are 200,000 to 500,000 cases of life-threatening dengue hemorrhagic fever (DHF) and dengue shock syndrome (DSS). Factors contributing to the development of DHF/DSS are not yet fully identified. Glucose-6-phosphate dehydrogenase (G6PD) deficiency is prevalent in Southeast Asian countries where dengue is also endemic. Besides affecting normal function of erythrocytes, G6PD deficiency also affects other cells by causing abnormal cellular redox. Altered redox state of cells may render them less effective in clearing up microbial and viral infections. Here we confirm previous findings that monocytes from G6PD-deficinet individuals support better dengue virus replication. In addition, we show that reduced production of reactive oxygen, and nitrogen species and elevated levels of oxidative stress are responsible for the enhanced viral replication. We suggest that redox imbalance observed in infected monocytes from G6PD-deficient individuals may facilitate dengue transmission and affect clinical outcome. However, a handful of studies carried out in areas where both G6PD deficiency and dengue are endemic, reveal no statistically significant correlation between severity of Dengue and G6PD deficiency. Well-designed studies are needed to demonstrate that G6PD-deficient individuals are at risk of severe dengue.</p></abstract><funding-group><funding-statement>This work was supported by Advanced Medical and Dental Institute (AMDI), Universiti Sains Malaysia (USM) under grant number USM/AMDI/2000/G-2/I and also the Post-graduate Student Fund, USM. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement></funding-group><counts><page-count count="9"></page-count></counts></article-meta></front></pmc><affiliations><list><country><li>Malaisie</li></country></list><tree><country name="Malaisie"><noRegion><name sortKey="Al Alimi, Abdullah Ahmed" sort="Al Alimi, Abdullah Ahmed" uniqKey="Al Alimi A" first="Abdullah Ahmed" last="Al-Alimi">Abdullah Ahmed Al-Alimi</name></noRegion><name sortKey="Al Hassan, Faisal Muti" sort="Al Hassan, Faisal Muti" uniqKey="Al Hassan F" first="Faisal Muti" last="Al-Hassan">Faisal Muti Al-Hassan</name><name sortKey="Ali, Syed A" sort="Ali, Syed A" uniqKey="Ali S" first="Syed A." last="Ali">Syed A. Ali</name><name sortKey="Idris, Fauziah Mohd" sort="Idris, Fauziah Mohd" uniqKey="Idris F" first="Fauziah Mohd" last="Idris">Fauziah Mohd Idris</name><name sortKey="Mohd Yusoff, Narazah" sort="Mohd Yusoff, Narazah" uniqKey="Mohd Yusoff N" first="Narazah" last="Mohd Yusoff">Narazah Mohd Yusoff</name><name sortKey="Teow, Sin Yeang" sort="Teow, Sin Yeang" uniqKey="Teow S" first="Sin-Yeang" last="Teow">Sin-Yeang Teow</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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