Journal of Neuroimmunology
Volume 178, Issue 1 , Pages 9-16 , September 2006

CCR2 mediates increases in glial activation caused by exposure to HIV-1 Tat and opiates

  • Nazira El-Hage

      Affiliations

    • Department of Anatomy and Neurobiology, University of Kentucky Medical Center, Lexington, KY 40536, USA
  • ,
  • Guanghan Wu

      Affiliations

    • Department of Anatomy and Neurobiology, University of Kentucky Medical Center, Lexington, KY 40536, USA
  • ,
  • Jayakrishna Ambati

      Affiliations

    • Department of Ophthalmology and Visual Sciences, University of Kentucky Medical Center, Lexington, KY 40536, USA
  • ,
  • Annadora J. Bruce-Keller

      Affiliations

    • Department of Anatomy and Neurobiology, University of Kentucky Medical Center, Lexington, KY 40536, USA
    • KY Spinal Cord and Brain Injury Research Center, University of Kentucky Medical Center, Lexington, KY 40536, USA
  • ,
  • Pamela E. Knapp

      Affiliations

    • Department of Anatomy and Neurobiology, University of Kentucky Medical Center, Lexington, KY 40536, USA
    • KY Spinal Cord and Brain Injury Research Center, University of Kentucky Medical Center, Lexington, KY 40536, USA
  • ,
  • Kurt F. Hauser

      Affiliations

    • Department of Anatomy and Neurobiology, University of Kentucky Medical Center, Lexington, KY 40536, USA
    • KY Spinal Cord and Brain Injury Research Center, University of Kentucky Medical Center, Lexington, KY 40536, USA
    • Corresponding Author InformationCorresponding author. Department of Anatomy and Neurobiology, University of Kentucky College of Medicine, 800 Rose Street, Lexington, KY 40536-0298, USA. Tel.: +1 859 323 6477; fax: +1 859 323 5946.

Received 28 December 2005 ,Revised 23 May 2006 ,Accepted 26 May 2006.

References 

  1. Ambati J, Anand A, Fernandez S, Sakurai E, Lynn BC, Kuziel WA, et al. An animal model of age-related macular degeneration in senescent Ccl-2- or Ccr-2-deficient mice. Nat. Med. 2003;9:1390–1397
  2. Andjelkovic AV, Kerkovich D, Shanley J, Pulliam L, Pachter JS. Expression of binding sites for beta chemokines on human astrocytes. Glia. 1999;28:225–235
  3. Andjelkovic AV, Song L, Dzenko KA, Cong H, Pachter JS. Functional expression of CCR2 by human fetal astrocytes. J. Neurosci. Res. 2002;70:219–231
  4. Avison MJ, Nath A, Greene-Avison R, Schmitt FA, Bales RA, Ethisham A, et al. Inflammatory changes and breakdown of microvascular integrity in early human immunodeficiency virus dementia. J. Neurovirology. 2004;10:223–232
  5. Banisadr G, Queraud-Lesaux F, Boutterin MC, Pelaprat D, Zalc B, Rostene W, et al. Distribution, cellular localization and functional role of CCR2 chemokine receptors in adult rat brain. J. Neurochem. 2002;81:257–269
  6. Bansal AK, Mactutus CF, Nath A, Maragos W, Hauser KF, Booze RM. Neurotoxicity of HIV-1 proteins gp120 and tat in the rat striatum. Brain Res. 2000;879:42–49
  7. Brouwer N, Zuurman MW, Wei T, Ransohoff RM, Boddeke HW, Biber K. Induction of glial L-CCR mRNA expression in spinal cord and brain in experimental autoimmune encephalomyelitis. Glia. 2004;46:84–94
  8. Chang L, Ernst T, St. Hillaire C, Conant K. Antiretroviral treatment alters relationship between MCP-1 and neurometabolites in HIV patients. Antivir. Ther. 2004;9:431–440
  9. Conant K, Garzino-Demo A, Nath A, McArthur JC, Halliday W, Power C, et al. Induction of monocyte chemoattractant protein-1 in HIV-1 Tat-stimulated astrocytes and elevation in AIDS dementia. Proc. Natl. Acad. Sci. U. S. A. 1998;95:3117–3121
  10. Croitoru-Lamoury J, Guillemin GJ, Boussin FD, Mognetti B, Gigout LI, Cheret A, et al. Expression of chemokines and their receptors in human and simian astrocytes: evidence for a central role of TNF alpha and IFN gamma in CXCR4 and CCR5 modulation. Glia. 2003;41:354–370
  11. Dorf ME, Berman MA, Tanabe S, Heesen M, Luo Y. Astrocytes express functional chemokine receptors. J. Neuroimmunol. 2000;111:109–121
  12. El-Hage N, Gurwell JA, Singh IN, Knapp PE, Nath A, Hauser KF. Synergistic increases in intracellular Ca2+, and the release of MCP-1, RANTES, and IL-6 by astrocytes treated with opiates and HIV-1 Tat. Glia. 2005;50:91–106
  13. El-Hage N, Wu G, Wang J, Ambati J, Knapp PE, Reed JL, et al. HIV-1 Tat and opiate-induced changes in astrocytes promote chemotaxis of microglia through the expression of MCP-1 and alternative chemokines. Glia. 2006;53:132–146
  14. Eriksson PS, Hansson E, Rönnbäck L. Mu and delta opiate receptors in neuronal and astroglial primary cultures from various regions of the brain-coupling with adenylate cyclase, localisation on the same neurones and association with dopamine (D1) receptor adenylate cyclase. Neuropharmacology. 1991;30:1233–1239
  15. Gonzalez E, Rovin BH, Sen L, Cooke G, Dhanda R, Mummidi S, et al. HIV-1 infection and AIDS dementia are influenced by a mutant MCP-1 allele linked to increased monocyte infiltration of tissues and MCP-1 levels. Proc. Natl. Acad. Sci. U. S. A. 2002;99:13795–13800
  16. Gurwell JA, Nath A, Sun Q, Zhang J, Martin KM, Chen Y, et al. Synergistic neurotoxicity of opioids and human immunodeficiency virus-1 Tat protein in striatal neurons in vitro. Neuroscience. 2001;102:555–563
  17. Hauser KF, Mangoura D. Diversity of the endogenous opioid system in development: novel signal transduction translates multiple extracellular signals into neural cell growth and differentiation. Perspect. Dev. Neurobiol. 1998;5:437–449
  18. Hauser KF, Stiene-Martin A, Mattson MP, Elde RP, Ryan SE, Godleske CC. μ-Opioid receptor-induced Ca2+ mobilization and astroglial development: Morphine inhibits DNA synthesis and stimulates cellular hypertrophy through a Ca2+-dependent mechanism. Brain Res. 1996;720:191–203
  19. Hauser KF, El-Hage N, Buch S, Berger JR, Tyor WR, Nath A, et al. Molecular targets of opiate drug abuse in neuroAIDS. Neurotox. Res. 2005;8:63–80
  20. Hauser KF, El-Hage N, Buch S, Tyor WR, Nath A, Bruce-Keller AJ, et al. Impact of opiate–HIV-1 interactions on neurotoxic signaling. J. Neuroimmune Pharmacol. 2006;1:98–105
  21. Hayashi M, Luo Y, Laning J, Strieter RM, Dorf ME. Production and function of monocyte chemoattractant protein-1 and other beta-chemokines in murine glial cells. J. Neuroimmunol. 1995;60:143–150
  22. Kaul M, Garden GA, Lipton SA. Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature. 2001;410:988–994
  23. Letendre S, Marquie-Beck J, Singh KK, de Almeida S, Zimmerman J, Spector SA, et al. The monocyte chemotactic protein-1-2578G allele is associated with elevated MCP-1 concentrations in cerebrospinal fluid. J. Neuroimmunol. 2004;157:193–196
  24. Ma M, Wei T, Boring L, Charo IF, Ransohoff RM, Jakeman LB. Monocyte recruitment and myelin removal are delayed following spinal cord injury in mice with CCR2 chemokine receptor deletion. J. Neurosci. Res. 2002;68:691–702
  25. Mahad DJ, Ransohoff RM. The role of MCP-1 (CCL2) and CCR2 in multiple sclerosis and experimental autoimmune encephalomyelitis (EAE). Semin. Immunol. 2003;15:23–32
  26. Mahajan SD, Aalinkeel R, Reynolds JL, Nair BB, Fernandez SF, Schwartz SA, et al. Morphine exacerbates HIV-1 viral protein gp120 induced modulation of chemokine gene expression in U373 astrocytoma cells. Curr. HIV Res. 2005;3:277–288
  27. Malik AA, Radhakrishnan N, Reddy K, Smith AD, Singhal PC. Morphine-induced macrophage apoptosis modulates migration of macrophages: use of in vitro model of urinary tract infection. J. Endourol. 2002;16:605–610
  28. Mankowski JL, Queen SE, Clements JE, Zink MC. Cerebrospinal fluid markers that predict SIV CNS disease. J. Neuroimmunol. 2004;157:66–70
  29. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 2004;25:677–686
  30. McManus CM, Weidenheim K, Woodman SE, Nunez J, Hesselgesser J, Nath A, et al. Chemokine and chemokine-receptor expression in human glial elements: induction by the HIV protein, Tat, and chemokine autoregulation. Am. J. Pathol. 2000;156:1441–1453
  31. Nath A. Pathobiology of human immunodeficiency virus dementia. Semin. Neurol. 1999;19:113–127
  32. Oh JW, Schwiebert LM, Benveniste EN. Cytokine regulation of CC and CXC chemokine expression by human astrocytes. J. Neurovirol. 1999;5:82–94
  33. Peterson PK, Hu S, Salak-Johnson J, Molitor TW, Chao CC. Differential production of and migratory response to beta chemokines by human microglia and astrocytes. J. Infect. Dis. 1997;175:478–481
  34. Petito CK, Roberts B, Cantando JD, Rabinstein A, Duncan R. Hippocampal injury and alterations in neuronal chemokine co-receptor expression in patients with AIDS. J. Neuropathol. Exp. Neurol. 2001;60:377–385
  35. Ransohoff RM, Hamilton TA, Tani M, Stoler MH, Shick HE, Major JA, et al. Astrocyte expression of mRNA encoding cytokines IP-10 and JE/MCP-1 in experimental autoimmune encephalomyelitis. FASEB J. 1993;7:592–600
  36. Rogers TJ, Peterson PK. Opioid G protein-coupled receptors: signals at the crossroads of inflammation. Trends Immunol. 2003;24:116–121
  37. Sevigny JJ, Albert SM, McDermott MP, McArthur JC, Sacktor N, Conant K, et al. Evaluation of HIV RNA and markers of immune activation as predictors of HIV-associated dementia. Neurology. 2004;63:2084–2090
  38. Simpson J, Rezaie P, Newcombe J, Cuzner ML, Male D, Woodroofe MN. Expression of the beta-chemokine receptors CCR2, CCR3 and CCR5 in multiple sclerosis central nervous system tissue. J. Neuroimmunol. 2000;108:192–200
  39. Singh KK, Ellis RJ, Marquie-Beck J, Letendre S, Heaton RK, Grant I, et al. CCR2 polymorphisms affect neuropsychological impairment in HIV-1-infected adults. J. Neuroimmunol. 2004;157:185–192
  40. Singhal PC, Shan ZH, Garg P, Sharma K, Sharma P, Gibbons N. Morphine modulates migration of monocytes. Nephron. 1996;73:526–531
  41. Stiene-Martin A, Hauser KF. Glial growth is regulated by agonists selective for multiple opioid receptor types in vitro. J. Neurosci. Res. 1991;29:538–548
  42. Stiene-Martin A, Zhou R, Hauser KF. Regional, developmental, and cell cycle-dependent differences in μ, δ, and κ-opioid receptor expression among cultured mouse astrocytes. Glia. 1998;22:249–259
  43. Stiene-Martin A, Knapp PE, Martin K, Gurwell JA, Ryan S, Thornton SR, et al. Opioid system diversity in developing neurons, astroglia, and oligodendroglia in the subventricular zone and striatum: impact on gliogenesis in vivo. Glia. 2001;36:78–88
  44. Szabo I, Wetzel MA, Zhang N, Steele AD, Kaminsky DE, Chen C, et al. Selective inactivation of CCR5 and decreased infectivity of R5 HIV-1 strains mediated by opioid-induced heterologous desensitization. J. Leukoc. Biol. 2003;74:1074–1082
  45. Zuurman MW, Heeroma J, Brouwer N, Boddeke HW, Biber K. LPS-induced expression of a novel chemokine receptor (L-CCR) in mouse glial cells in vitro and in vivo. Glia. 2003;41:327–336

PII: S0165-5728(06)00209-8

doi: 10.1016/j.jneuroim.2006.05.027

Journal of Neuroimmunology
Volume 178, Issue 1 , Pages 9-16 , September 2006