Toll-Like Receptor-3 Mediates HIV-1-Induced Interleukin-6 Expression in the Human Brain Endothelium via TAK1 and JNK Pathways: Implications for Viral Neuropathogenesis

HIV-1-associated neurocognitive disorders (HAND) is associated with blood-brain-barrier (BBB) inflammation, and inflammation involves toll-like receptors (TLRs) signaling. It is not known whether primary human brain microvascular endothelial cells (HBMEC), the major BBB component, express TLRs or wh...

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Published inMolecular neurobiology Vol. 55; no. 7; pp. 5976 - 5992
Main Authors Bhargavan, Biju, Kanmogne, Georgette D.
Format Journal Article
LanguageEnglish
Published New York Springer US 01.07.2018
Springer Nature B.V
Subjects
Acquired immune deficiency syndrome
Adult
Aged
AIDS
Biomedical and Life Sciences
Biomedicine
Blood vessels
Blood-brain barrier
Brain
Brain - pathology
c-Jun protein
Cell activation
Cell Biology
Cognition
Cytokines
Endothelial cells
Endothelial Cells - metabolism
Endothelial Cells - pathology
Endothelial Cells - virology
Endothelium
Female
HIV
HIV Infections - genetics
HIV Infections - pathology
HIV-1 - physiology
Human immunodeficiency virus
Humans
Inflammation
Interleukin 1
Interleukin 6
Interleukin-6 - genetics
Interleukin-6 - metabolism
Leukocyte migration
Ligands
Male
MAP Kinase Kinase Kinases - metabolism
MAP Kinase Signaling System
Microvasculature
Middle Aged
Models, Biological
Monocytes
Neurobiology
Neurology
Neuropathogenesis
Neurosciences
Phosphorylation
RNA, Double-Stranded - metabolism
RNA, Messenger - genetics
RNA, Messenger - metabolism
Serine
Stat1 protein
TAK1 protein
TLR3 protein
Toll-Like Receptor 3 - genetics
Toll-Like Receptor 3 - metabolism
Toll-like receptors
Transcription activation
Transcription factors
Transcription, Genetic
Up-Regulation - genetics
HIV-1
IL6
Monocytes
Blood-brain barrier
Claudin-5
TAK1/MKK7/JNK signaling
Human brain microvascular endothelial cells
TLR3
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Abstract HIV-1-associated neurocognitive disorders (HAND) is associated with blood-brain-barrier (BBB) inflammation, and inflammation involves toll-like receptors (TLRs) signaling. It is not known whether primary human brain microvascular endothelial cells (HBMEC), the major BBB component, express TLRs or whether TLRs are involved in BBB dysfunction and HAND. We demonstrate that HBMEC express TLR3, 4, 5, 7, 9, and 10, and TLR3 was the most abundant. HIV-1 and TLR3 activation increased endothelial TLR3 transcription and expression. HIV-1-positive human subjects showed significantly higher TLR3 expression in brain tissues and blood vessels, with higher TLR3 levels in subjects with HAND. HIV-1 and TLR3 activation increased endothelial IL6 expression by 6-to-127-fold ( P  < 0.001), activated c-jun(serine-63) and SAPK/JNK(Thr183/Tyr185). HIV-1 upregulated IL6 through interleukin-1 receptor-associated-kinase (IRAK)-1/4/TAK1/JNK pathways, via ATP-dependent JNK activation. TLR3 activation upregulated IL6 through TAK1/JNK pathways, via ATP-dependent or -independent JNK activation. HIV-1 and TLR3 activation also upregulated transcription factors associated with IL6 and TAK1/JNK pathways (Jun, CEBPA, STAT1). Blocking TLR3 activation prevented HIV-1- and TLR3 ligands-induced upregulation of these transcription factors, prevented IL6 transcription and expression, c-jun and JNK activation. HIV-1 and TLR3 ligands significantly increased monocytes adhesion and migration through the BBB, and decreased endothelial claudin-5 expression. Blocking TLR3 and JNK activation prevented HIV-1- and TLR3 ligands-induced claudin-5 downregulation, monocytes adhesion and transendothelial migration. These data suggest that viral immune recognition via endothelial TLR3 is involved in endothelial inflammation and BBB dysfunction in HIV/AIDS and HAND. Our data provides novel insights into the molecular basis of these HIV-1- and TLR3-mediated effects.
AbstractList HIV-1-associated neurocognitive impairment (HAND) is associated with blood-brain-barrier (BBB) inflammation, and inflammation involves toll-like receptors (TLRs) signaling. It is not known whether primary human brain microvascular endothelial cells (HBMEC), the major BBB component, express TLRs or whether TLRs are involved in BBB dysfunction and HAND. We demonstrate that HBMEC express TLR3, 4, 5, 7, 9, and 10, and TLR3 was the most abundant. HIV-1 and TLR3 activation increased endothelial TLR3 transcription and expression. HIV-1-positive human subjects showed significantly higher TLR3 expression in brain tissues and blood vessels, with higher TLR3 levels in subjects with HAND. HIV-1 and TLR3 activation increased endothelial IL6 expression by 6-to-127-fold ( P <0.001), activated c-jun(serine-63) and SAPK/JNK(Thr183/Tyr185). HIV-1 upregulated IL6 through interleukin-1 receptor-associated-kinase(IRAK)-1/4/TAK1/JNK pathways, via ATP-dependent JNK activation. TLR3 activation upregulated IL6 through TAK1/JNK pathways, via ATP-dependent or -independent JNK activation. HIV-1 and TLR3 activation also upregulated transcription factors associated with IL6 and TAK1/JNK pathways (Jun, CEBPA, STAT1). Blocking TLR3 activation prevented HIV-1-and TLR3 ligands-induced upregulation of these transcription factors, prevented IL6 transcription and expression, c-jun and JNK activation. HIV-1 and TLR3 ligands significantly increased monocytes adhesion and migration through the BBB, and decreased endothelial claudin-5 expression. Blocking TLR3 and JNK activation prevented HIV-1- and TLR3 ligands-induced claudin-5 downregulation, monocytes adhesion and transendothelial migration. These data suggests that viral immune recognition via endothelial TLR3 is involved in endothelial inflammation and BBB dysfunction in HIV/AIDS and HAND. Our data provides novel insights into the molecular basis of these HIV-1- and TLR3-mediated effects.
HIV-1-associated neurocognitive disorders (HAND) is associated with blood-brain-barrier (BBB) inflammation, and inflammation involves toll-like receptors (TLRs) signaling. It is not known whether primary human brain microvascular endothelial cells (HBMEC), the major BBB component, express TLRs or whether TLRs are involved in BBB dysfunction and HAND. We demonstrate that HBMEC express TLR3, 4, 5, 7, 9, and 10, and TLR3 was the most abundant. HIV-1 and TLR3 activation increased endothelial TLR3 transcription and expression. HIV-1-positive human subjects showed significantly higher TLR3 expression in brain tissues and blood vessels, with higher TLR3 levels in subjects with HAND. HIV-1 and TLR3 activation increased endothelial IL6 expression by 6-to-127-fold ( P  < 0.001), activated c-jun(serine-63) and SAPK/JNK(Thr183/Tyr185). HIV-1 upregulated IL6 through interleukin-1 receptor-associated-kinase (IRAK)-1/4/TAK1/JNK pathways, via ATP-dependent JNK activation. TLR3 activation upregulated IL6 through TAK1/JNK pathways, via ATP-dependent or -independent JNK activation. HIV-1 and TLR3 activation also upregulated transcription factors associated with IL6 and TAK1/JNK pathways (Jun, CEBPA, STAT1). Blocking TLR3 activation prevented HIV-1- and TLR3 ligands-induced upregulation of these transcription factors, prevented IL6 transcription and expression, c-jun and JNK activation. HIV-1 and TLR3 ligands significantly increased monocytes adhesion and migration through the BBB, and decreased endothelial claudin-5 expression. Blocking TLR3 and JNK activation prevented HIV-1- and TLR3 ligands-induced claudin-5 downregulation, monocytes adhesion and transendothelial migration. These data suggest that viral immune recognition via endothelial TLR3 is involved in endothelial inflammation and BBB dysfunction in HIV/AIDS and HAND. Our data provides novel insights into the molecular basis of these HIV-1- and TLR3-mediated effects.
HIV-1-associated neurocognitive disorders (HAND) is associated with blood-brain-barrier (BBB) inflammation, and inflammation involves toll-like receptors (TLRs) signaling. It is not known whether primary human brain microvascular endothelial cells (HBMEC), the major BBB component, express TLRs or whether TLRs are involved in BBB dysfunction and HAND. We demonstrate that HBMEC express TLR3, 4, 5, 7, 9, and 10, and TLR3 was the most abundant. HIV-1 and TLR3 activation increased endothelial TLR3 transcription and expression. HIV-1-positive human subjects showed significantly higher TLR3 expression in brain tissues and blood vessels, with higher TLR3 levels in subjects with HAND. HIV-1 and TLR3 activation increased endothelial IL6 expression by 6-to-127-fold (P < 0.001), activated c-jun(serine-63) and SAPK/JNK(Thr183/Tyr185). HIV-1 upregulated IL6 through interleukin-1 receptor-associated-kinase (IRAK)-1/4/TAK1/JNK pathways, via ATP-dependent JNK activation. TLR3 activation upregulated IL6 through TAK1/JNK pathways, via ATP-dependent or -independent JNK activation. HIV-1 and TLR3 activation also upregulated transcription factors associated with IL6 and TAK1/JNK pathways (Jun, CEBPA, STAT1). Blocking TLR3 activation prevented HIV-1- and TLR3 ligands-induced upregulation of these transcription factors, prevented IL6 transcription and expression, c-jun and JNK activation. HIV-1 and TLR3 ligands significantly increased monocytes adhesion and migration through the BBB, and decreased endothelial claudin-5 expression. Blocking TLR3 and JNK activation prevented HIV-1- and TLR3 ligands-induced claudin-5 downregulation, monocytes adhesion and transendothelial migration. These data suggest that viral immune recognition via endothelial TLR3 is involved in endothelial inflammation and BBB dysfunction in HIV/AIDS and HAND. Our data provides novel insights into the molecular basis of these HIV-1- and TLR3-mediated effects.HIV-1-associated neurocognitive disorders (HAND) is associated with blood-brain-barrier (BBB) inflammation, and inflammation involves toll-like receptors (TLRs) signaling. It is not known whether primary human brain microvascular endothelial cells (HBMEC), the major BBB component, express TLRs or whether TLRs are involved in BBB dysfunction and HAND. We demonstrate that HBMEC express TLR3, 4, 5, 7, 9, and 10, and TLR3 was the most abundant. HIV-1 and TLR3 activation increased endothelial TLR3 transcription and expression. HIV-1-positive human subjects showed significantly higher TLR3 expression in brain tissues and blood vessels, with higher TLR3 levels in subjects with HAND. HIV-1 and TLR3 activation increased endothelial IL6 expression by 6-to-127-fold (P < 0.001), activated c-jun(serine-63) and SAPK/JNK(Thr183/Tyr185). HIV-1 upregulated IL6 through interleukin-1 receptor-associated-kinase (IRAK)-1/4/TAK1/JNK pathways, via ATP-dependent JNK activation. TLR3 activation upregulated IL6 through TAK1/JNK pathways, via ATP-dependent or -independent JNK activation. HIV-1 and TLR3 activation also upregulated transcription factors associated with IL6 and TAK1/JNK pathways (Jun, CEBPA, STAT1). Blocking TLR3 activation prevented HIV-1- and TLR3 ligands-induced upregulation of these transcription factors, prevented IL6 transcription and expression, c-jun and JNK activation. HIV-1 and TLR3 ligands significantly increased monocytes adhesion and migration through the BBB, and decreased endothelial claudin-5 expression. Blocking TLR3 and JNK activation prevented HIV-1- and TLR3 ligands-induced claudin-5 downregulation, monocytes adhesion and transendothelial migration. These data suggest that viral immune recognition via endothelial TLR3 is involved in endothelial inflammation and BBB dysfunction in HIV/AIDS and HAND. Our data provides novel insights into the molecular basis of these HIV-1- and TLR3-mediated effects.
HIV-1-associated neurocognitive disorders (HAND) is associated with blood-brain-barrier (BBB) inflammation, and inflammation involves toll-like receptors (TLRs) signaling. It is not known whether primary human brain microvascular endothelial cells (HBMEC), the major BBB component, express TLRs or whether TLRs are involved in BBB dysfunction and HAND. We demonstrate that HBMEC express TLR3, 4, 5, 7, 9, and 10, and TLR3 was the most abundant. HIV-1 and TLR3 activation increased endothelial TLR3 transcription and expression. HIV-1-positive human subjects showed significantly higher TLR3 expression in brain tissues and blood vessels, with higher TLR3 levels in subjects with HAND. HIV-1 and TLR3 activation increased endothelial IL6 expression by 6-to-127-fold (P < 0.001), activated c-jun(serine-63) and SAPK/JNK(Thr183/Tyr185). HIV-1 upregulated IL6 through interleukin-1 receptor-associated-kinase (IRAK)-1/4/TAK1/JNK pathways, via ATP-dependent JNK activation. TLR3 activation upregulated IL6 through TAK1/JNK pathways, via ATP-dependent or -independent JNK activation. HIV-1 and TLR3 activation also upregulated transcription factors associated with IL6 and TAK1/JNK pathways (Jun, CEBPA, STAT1). Blocking TLR3 activation prevented HIV-1- and TLR3 ligands-induced upregulation of these transcription factors, prevented IL6 transcription and expression, c-jun and JNK activation. HIV-1 and TLR3 ligands significantly increased monocytes adhesion and migration through the BBB, and decreased endothelial claudin-5 expression. Blocking TLR3 and JNK activation prevented HIV-1- and TLR3 ligands-induced claudin-5 downregulation, monocytes adhesion and transendothelial migration. These data suggest that viral immune recognition via endothelial TLR3 is involved in endothelial inflammation and BBB dysfunction in HIV/AIDS and HAND. Our data provides novel insights into the molecular basis of these HIV-1- and TLR3-mediated effects.
HIV-1-associated neurocognitive disorders (HAND) is associated with blood-brain-barrier (BBB) inflammation, and inflammation involves toll-like receptors (TLRs) signaling. It is not known whether primary human brain microvascular endothelial cells (HBMEC), the major BBB component, express TLRs or whether TLRs are involved in BBB dysfunction and HAND. We demonstrate that HBMEC express TLR3, 4, 5, 7, 9, and 10, and TLR3 was the most abundant. HIV-1 and TLR3 activation increased endothelial TLR3 transcription and expression. HIV-1-positive human subjects showed significantly higher TLR3 expression in brain tissues and blood vessels, with higher TLR3 levels in subjects with HAND. HIV-1 and TLR3 activation increased endothelial IL6 expression by 6-to-127-fold (P < 0.001), activated c-jun(serine-63) and SAPK/JNK(Thr183/Tyr185). HIV-1 upregulated IL6 through interleukin-1 receptor-associated-kinase (IRAK)-1/4/TAK1/JNK pathways, via ATP-dependent JNK activation. TLR3 activation upregulated IL6 through TAK1/JNK pathways, via ATP-dependent or -independent JNK activation. HIV-1 and TLR3 activation also upregulated transcription factors associated with IL6 and TAK1/JNK pathways (Jun, CEBPA, STAT1). Blocking TLR3 activation prevented HIV-1- and TLR3 ligands-induced upregulation of these transcription factors, prevented IL6 transcription and expression, c-jun and JNK activation. HIV-1 and TLR3 ligands significantly increased monocytes adhesion and migration through the BBB, and decreased endothelial claudin-5 expression. Blocking TLR3 and JNK activation prevented HIV-1- and TLR3 ligands-induced claudin-5 downregulation, monocytes adhesion and transendothelial migration. These data suggest that viral immune recognition via endothelial TLR3 is involved in endothelial inflammation and BBB dysfunction in HIV/AIDS and HAND. Our data provides novel insights into the molecular basis of these HIV-1- and TLR3-mediated effects.
Author Bhargavan, Biju
Kanmogne, Georgette D.
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  surname: Kanmogne
  fullname: Kanmogne, Georgette D.
  email: gkanmogne@unmc.edu
  organization: Department of Pharmacology and Experimental Neuroscience, University of Nebraska Medical Center
BackLink https://www.ncbi.nlm.nih.gov/pubmed/29128906$$D View this record in MEDLINE/PubMed
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Copyright Springer Science+Business Media, LLC 2017
Molecular Neurobiology is a copyright of Springer, (2017). All Rights Reserved.
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ISSN 0893-7648
1559-1182
IngestDate Thu Aug 21 14:25:47 EDT 2025
Fri Jul 11 11:50:19 EDT 2025
Fri Jul 25 09:24:24 EDT 2025
Mon Jul 21 05:58:11 EDT 2025
Tue Jul 01 01:04:41 EDT 2025
Thu Apr 24 23:08:29 EDT 2025
Fri Feb 21 02:38:15 EST 2025
IsPeerReviewed true
IsScholarly true
Issue 7
Keywords HIV-1
IL6
Monocytes
Blood-brain barrier
Claudin-5
TAK1/MKK7/JNK signaling
Human brain microvascular endothelial cells
TLR3
Language English
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springer_journals_10_1007_s12035_017_0816_8
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PublicationTitle Molecular neurobiology
PublicationTitleAbbrev Mol Neurobiol
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Publisher Springer US
Springer Nature B.V
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Snippet HIV-1-associated neurocognitive disorders (HAND) is associated with blood-brain-barrier (BBB) inflammation, and inflammation involves toll-like receptors...
HIV-1-associated neurocognitive impairment (HAND) is associated with blood-brain-barrier (BBB) inflammation, and inflammation involves toll-like receptors...
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pubmed
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StartPage 5976
SubjectTerms Acquired immune deficiency syndrome
Adult
Aged
AIDS
Biomedical and Life Sciences
Biomedicine
Blood vessels
Blood-brain barrier
Brain
Brain - pathology
c-Jun protein
Cell activation
Cell Biology
Cognition
Cytokines
Endothelial cells
Endothelial Cells - metabolism
Endothelial Cells - pathology
Endothelial Cells - virology
Endothelium
Female
HIV
HIV Infections - genetics
HIV Infections - pathology
HIV-1 - physiology
Human immunodeficiency virus
Humans
Inflammation
Interleukin 1
Interleukin 6
Interleukin-6 - genetics
Interleukin-6 - metabolism
Leukocyte migration
Ligands
Male
MAP Kinase Kinase Kinases - metabolism
MAP Kinase Signaling System
Microvasculature
Middle Aged
Models, Biological
Monocytes
Neurobiology
Neurology
Neuropathogenesis
Neurosciences
Phosphorylation
RNA, Double-Stranded - metabolism
RNA, Messenger - genetics
RNA, Messenger - metabolism
Serine
Stat1 protein
TAK1 protein
TLR3 protein
Toll-Like Receptor 3 - genetics
Toll-Like Receptor 3 - metabolism
Toll-like receptors
Transcription activation
Transcription factors
Transcription, Genetic
Up-Regulation - genetics
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Title Toll-Like Receptor-3 Mediates HIV-1-Induced Interleukin-6 Expression in the Human Brain Endothelium via TAK1 and JNK Pathways: Implications for Viral Neuropathogenesis
URI https://link.springer.com/article/10.1007/s12035-017-0816-8
https://www.ncbi.nlm.nih.gov/pubmed/29128906
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https://pubmed.ncbi.nlm.nih.gov/PMC6226278
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