Wingless-type mammary tumor virus integration site family, member 5A (Wnt5a) regulates human immunodeficiency virus type 1 (HIV-1) envelope glycoprotein 120 (gp120)-induced expression of pro-inflammatory cytokines via the Ca2+/calmodulin-dependent protein kinase II (CaMKII) and c-Jun N-terminal kinase (JNK) signaling pathways

J Biol Chem. 2013 May 10;288(19):13610-9. doi: 10.1074/jbc.M112.381046. Epub 2013 Mar 28.

Abstract

Background: HIV-1 infection causes chronic neuroinflammation in the central nervous system (CNS).

Results: The spinal cytokine up-regulation induced by HIV-1 gp120 protein depends on Wnt5a/CaMKII and/or Wnt5a/JNK pathways.

Conclusion: gp120 stimulates cytokine expression in the spinal cord dorsal horn by activating Wnt5a signaling.

Significance: The finding reveals Wnt signaling-mediated novel mechanisms by which HIV-1 may cause neuroinflammation. Chronic expression of pro-inflammatory cytokines critically contributes to the pathogenesis of HIV-associated neurological disorders (HANDs), but the host mechanism that regulates the HIV-induced cytokine expression in the CNS remains elusive. Here, we present evidence for a crucial role of Wnt5a signaling in the expression of pro-inflammatory cytokines in the spinal cord induced by a major HIV-envelope protein, gp120. Wnt5a is mainly expressed in spinal neurons, and rapidly up-regulated by intrathecal injection (i.t.) of gp120. We show that inhibition of Wnt5a by specific antagonists blocks gp120-induced up-regulation of IL-1β, IL-6, and TNF-α in the spinal cord. Conversely, injection (i.t.) of purified recombinant Wnt5a stimulates the expression of these cytokines. To elucidate the role of the Wnt5a-regulated signaling pathways in gp120-induced cytokine expression, we have focused on CaMKII and JNKs, the well characterized down-stream targets of Wnt5a signaling. We find that Wnt5a is required for gp120 to activate CaMKII and JNK signaling. Furthermore, we demonstrate that the Wnt5a/CaMKII pathway is critical for the gp120-induced expression of IL-1β, whereas the Wnt5a/JNK pathway is for TNF-α expression. Meanwhile, the expression of IL-6 is co-regulated by both pathways. These results collectively suggest that Wnt5a signaling cascades play a crucial role in the regulation of gp120-induced expression of pro-inflammatory cytokines in the CNS.

Keywords: CNS; Cytokine; HIV-1; Neurobiology; Neuroinflammation; Spinal Cord; Wnt Signaling; gp120.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / metabolism*
  • Cells, Cultured
  • Cytokines / genetics*
  • Cytokines / metabolism
  • HIV Envelope Protein gp120 / metabolism*
  • HIV Envelope Protein gp120 / physiology
  • Humans
  • Inflammation Mediators / metabolism
  • JNK Mitogen-Activated Protein Kinases / metabolism
  • MAP Kinase Signaling System*
  • Mice
  • Mice, Inbred C57BL
  • Neural Stem Cells / metabolism
  • Spinal Cord / metabolism
  • Transcriptional Activation
  • Up-Regulation
  • Wnt Proteins / antagonists & inhibitors
  • Wnt Proteins / genetics
  • Wnt Proteins / metabolism*
  • Wnt-5a Protein

Substances

  • Cytokines
  • HIV Envelope Protein gp120
  • Inflammation Mediators
  • Wnt Proteins
  • Wnt-5a Protein
  • Wnt5a protein, mouse
  • gp120 protein, Human immunodeficiency virus 1
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • JNK Mitogen-Activated Protein Kinases