Morphine exacerbates HIV-1 Tat-induced cytokine production in astrocytes through convergent effects on [Ca2+]i, NF-κB trafficking and transcription

PLoS ONE

Volumn 3, Issue 12, 2008, Pages

  El Hage, Nazira ^a   Bruce Keller, Annadora J ^b   Yakovleva, Tatiana ^c   Bazov, Igor ^c   Bakalkin, Georgy ^c   Knapp, Pamela E ^a,d   Hauser, Kurt F ^a,d  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^c UPPSALA UNIVERSITY   (Sweden)

^d VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CHEMOKINE; CYTOKINE; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; LEPTOMYCIN B; MONOCYTE CHEMOTACTIC PROTEIN 1; MORPHINE SULFATE; PARTHENOLIDE; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR REL; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; CALCIUM; MORPHINE; NARCOTIC ANALGESIC AGENT;

ANIMAL CELL; ARTICLE; ASTROCYTE; CALCIUM BINDING; CALCIUM CELL LEVEL; CELL FUNCTION; CELL NUCLEUS; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENCEPHALITIS; HUMAN IMMUNODEFICIENCY VIRUS 1; MOUSE; NEUROPATHOLOGY; NONHUMAN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ANIMAL; BIOLOGICAL MODEL; BIOSYNTHESIS; CYTOPLASM; DRUG EFFECT; GENETIC TRANSCRIPTION; GENETICS; IMMUNOLOGY; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; PROTO ONCOGENE;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ANALGESICS, OPIOID; ANIMALS; ASTROCYTES; CALCIUM; CELL NUCLEUS; CYTOKINES; CYTOPLASM; GENES, REL; HIV-1; MICE; MICE, INBRED ICR; MODELS, BIOLOGICAL; MORPHINE; NF-KAPPA B; SIGNAL TRANSDUCTION; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; TRANSCRIPTION, GENETIC; TUMOR NECROSIS FACTOR-ALPHA;

EID: 58149339916     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0004093     Document Type: Article

References (60)

1. Bell JE, Brettle RP, Chiswick A, Simmonds P (1998) HIV encephalitis, proviral load and dementia in drug users and homosexuals with AIDS. Effect of neocortical involvement. Brain 121: 2043-2052.
2. Nath A, Maragos WF, Avison MJ, Schmitt FA, Berger JR (2001) Acceleration of HIV dementia with methamphetamine and cocaine. J Neurovirol 7: 66-71.
3. Bell JE, Anthony JC, Simmonds P (2006) Impact of HIV on regional and cellular organization of the brain. Curr HIV Res 4: 249-257.
4. Nath A, Jones M, Maragos W, Booze R, Mactutus C, et al. (2000) Neurotoxicity and dysfunction of dopamine systems associated with AIDS dementia. Psychopharmacol 14: 222-227.
5. Nath A, Hauser KF, Wojna V, Booze RM, Maragos W, et al. (2002) Molecular basis for interactions of HIV and drugs of abuse. J Acquir Immune Defic Syndr 31 Suppl 2: S62-S69.
6. Hauser KF, El-Hage N, Buch S, Berger JR, Tyor WR, et al. (2005) Molecular targets of opiate drug abuse in NeuroAids. Neurotox Res 8: 63-80.
7. Mahajan SD, Schwartz SA, Shanahan TC, Chawda RP, Nair MP (2002) Morphine regulates gene expression of alpha- and beta-chemokines and their receptors on astroglial cells via the opioid mu receptor. J Immunol 169: 3589-3599.
8. Mahajan SD, Stanley A, Schwartz A, Aalinkeel R, Chawda RP, et al. (2005) Morphine modulates chemokine gene regulation in normal human astrocytes. Clin Immunol 115: 323-332.
9. 1-72 and opiate-induced changes in astrocytes promote chemotaxis of microglia through the expression of MCP-1 and alternative chemokines. Glia 53: 132-146.
10. Song H, Stevens CF, Gage FH (2002) Astroglia induce neurogenesis from adult neural stem cells. Nature 417: 39-44.
11. Araque A, Parpura V, Sanzgiri RP, Haydon PG (1999) Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci 22: 208-215.
12. Garcia-Segura LM, Naftolin F, Hutchison JB, Azcoitia I, Chowen JA (1999) Role of astroglia in estrogen regulation of synaptic plasticity and brain repair. J Neurobiol 40: 574-584.
13. Prat A, Biernacki K, Wosik K, Antel JP (2001) Glial cell influence on the human blood-brain barrier. Glia 36: 145-155.
14. Dong Y, Benveniste EN (2001) Immune function of astrocytes. Glia 36: 180-190.
15. Allan SM, Rothwell NJ (2003) Inflammation in central nervous system. Philos Trans R Soc Lond B Biol Sci 358: 1669-1677.
16. Luo Y, Berman MA, Abromson-Leeman SR, Dorf ME (2003) Tumor necrosis factor is required for RANTES-induced astrocyte monocyte chemoattractant protein-1 production. Glia 43: 119-127.
17. 2+, and the release of MCP-1, RANTES and IL-6 by astrocytes treated with opiates and HIV-1 Tat. Glia 50: 91-106.
18. El-Hage N, Wu G, Ambati J, Bruce-Keller A, Knapp PE, et al. (2006) CCR2 mediates increases in glial activation caused by exposure to HIV-1 Tat and opiates. J Neuroimmunol 178: 9-16.
19. Conant K, Garzino-Demo A, Nath A, McArthur JC, Halliday W, et al. (1998) Induction of monocyte chemoattractant protein-1 in HIV-1 Tat-stimulated astrocytes and elevation in AIDS dementia. Proc Natl Acad Sci U S A 95: 3117-3121.
20. Eugenin EA, Osiecki K, Lopez L, Goldstein H, Calderon TM, et al. (2006) CCL2/monocyte chemoattractant protein-1 mediates enhanced transmigration of human immunodeficiency virus (HIV)-infected leukocytes across the bloodbrain barrier: a potential mechanism of HIV-CNS invasion and NeuroAIDS. J Neurosci 26: 1098-1106.
21. Sevigny JJ, Albert SM, McDermott MP, McArthur JC, Sacktor N, et al. (2004) Evaluation of HIV RNA and markers of immune activation as predictors of HIV-associated dementia. Neurology 63: 2084-2090.
22. Mankowski JL, Queen SE, Clements JE, Zink MC (2004) Cerebrospinal fluid markers that predict SIV CNS disease. J Neuroimmunol 157: 66-70.
23. Tyor WR, Glass JD, Friffin JW (1992) Cytokine expression in the brain during AIDS. Ann Neurol 31: 349-360.
24. Fiala M, Rhodes RH, Shapshak P, Nagano I, Martinez-Maza O, et al. (1996) Regulation of HIV-1 infection in astrocytes: expression ofNef, TNF- alpha and IL-6 is enhanced in coculture of astrocytes with macrophages. J Neurovirol 2: 158-166.
25. Roy S, Cain KJ, Chapin RB, Charboneau RG, Barke RA (1998) Morphine modulates NF kappa B activation in macrophages. Biochem Biophys Res Commun 245: 392-396.
26. Hua LL, Zhao ML, Cosenza M, Kim MO, Huang H, et al. (2002) Role of mitogen-activated protein kinases in inducible nitric oxide synthase and TNFalpha expression in human fetal astrocytes. J Neuroimmunol 126: 180-189.
27. Kim JM, Oh YK, Lee JH, Im DY, Kim YJ, et al. (2005) Induction of proinflammatory mediators requires activation of the TRAF, NIK, IKK and NF-kappa B signal transduction pathway in astrocytes infected with Escherichia coli. Clin Exp Immunol 140: 450-160.
28. Quinones MP, Kalkonde Y, Estrada CA, Jimenez F, Ramirez R, et al. (2008) Role of astrocytes and chemokine systems in acute TNFalpha induced demyelinating syndrome: CCR2-dependent signals promote astrocyte activation and survival via NF-kappa B and Akt. Mol Cell Neurosci 37: 96-109.
29. Baeuerle PA, Baltimore D (1996) NF-kB: Ten years later. Cell 87: 13-20.
30. Wang D, Baldwin AS (1998) Activation of Nuclear Factor-κB-dependent transcription by tumor necrosis factor-alpha is mediated through phosphorylation of RelA/p65 on serine 529. J Biol Chem 273: 29411-29416.
31. Zhai Q, Luo Y, Zhang Y, Berman MA, Dorf ME (2004) Low nuclear levels of nuclear factor-kappa B are essential for KC self-induction in astrocytes: Requirements for shuttling and phosphorylation. Glia 48: 327-336.
32. O'Neill LA, Kalschmidt C (1997) NF-kappa B: a crucial transcription factor for glial and neuronal cell function. Trends Neurosci 20: 252-258.
33. Hayden MS, Ghosh S (2008) Shared principle in NF-kappa B signaling. Cell 132: 344-361.
34. Israël A (2000) The IKK complex: an integrator of all signals that activate NFkB? Trends in Cell Biol 10: 129-133.
35. Ghosh S, Karin M (2002) Missing pieces in the NF-kB puzzle. Cell 109: S81-S96.
36. Stiene-Martin A, Zhou R, Hauser KF (1998) Regional, developmental, and cell cycle-dependent differences in μ, δ, and κ-opioid receptor expression among cultured mouse astrocytes. Glia 22: 249-259.
37. 2+-dependent mechanism. Brain Res 720: 191-203.
38. Kuriyan J, Thanos D (1995) Structure of the NF-kB transcription factor: a holistic interaction with DNA. Curr Biol 3: 135-141.
39. Stylianou E, Nie M, Ueda A, Zhao L (1999) c-Rel and p65 trans-activate the monocyte chemoattractant protein gene in interleukin stimulated mesengial cells. Kidney Int 56: 873-882.
40. Lawrence DM, Seth P, Durham L, Diaz F, Boursiquot R, et al. (2006) Astrocyte differentiation selectively upregulates CCL2/monocyte chemoattractant protein-1 in cultured human brain-derived progenitor cells. Glia 53: 81-91.
41. Hehner SP, Hofmann TG, Droge W, Schmitz ML (1999) The antiinflammatory sesquiterpene lactone parthenolide inhibits NF-kappa B by targeting the I kappa B kinase complex. J Immunol 163: 5617-5623.
42. Kwok BH, Koh B, Ndubuisi MI, Elofsson M, Crews CM (2001) The anti-inflammatory natural product parthenolide from the medicinal herb Feverfew directly binds to and inhibits IkappaB kinase. Chem Biol 8: 759-766.
43. El-Hage N, Bruce-Keller AJ, Knapp PE, Hauser KF (2008) CCL5/RANTES gene deletion attenuates opioid-induced increases in glial CCL2/MCP-1 immunoreactivity and activation in HIV-1 Tat-exposed mice. J Neuroimmune Pharmacol 3: 275-285.
44. Swinney DC, Xu Y-Z, Scarafia LE, Lee I, Mak AY, et al. (2002) A small molecule ubiquitination inhibitor blocks NF-kB-dependent cytokine expression in cells and rats. J Biol Chem 277: 23573-23581.
45. Luo Y, Berman MA, Zhai Q, Fischer FR, Abromson-Leeman SR, et al. (2002) RANTES stimulates inflammatory cascades and receptor modulation in murine astrocytes. Glia 39: 19-30.
46. 2+ entry enhances muscarinic receptor-mediated soluble amyloid precursor protein (sAPPalpha) release in SH-SY5Y cells. J Biol Chem 281: 12722-12728.
47. Lilienbaum A, Israël A (2003) From calcium to NF-kB signaling pathways in neurons. Mol Cell Biol 23: 2680-2698.
48. Haughey NJ, Holden CP, Nath A, Geiger JD (1999) Involvement of inositol 1,4,5-trisphosphate-regulated stores of intracellular calcium in calcium dysregulation and neuron cell death caused by HIV-1 protein Tat. J Neurochem 73: 1363-1374.
49. Haughey NJ, Mattson MP (2002) Calcium dysregulation and neuronal apoptosis by the HIV-1 proteins Tat and gp120. J Acquir Immune Defic Syndr 31 Suppl 2: S55-S61.
50. Wolff B, Sanglier JJ, Wang Y (1997) Leptomycin B is an inhibitor of nuclear export: inhibition of nucleo-cytoplasmic translocation of the human immunodeficiency virus type 1 (HIV-1) Rev protein and Rev-dependent mRNA. Chem Biol 4: 139-147.
51. Adachi M, Fakuda M, Nishida E (2000) Nuclear export of MAP kinase (ERK) involves a MAP kinase (MEK)-dependent active transport mechanism. J Cell Biol 148: 849-856.
52. Birbach A, Gold P, Binder BR, Hofer E, de Martin R, et al. (2002) Signaling molecules of the NF-kB pathway shuttle constitutively between cytoplasm and nucleus. J Biol Chem 277: 10842-10851.
53. Arenzana-Seisdedos F, Thompson J, Rodriquez MS, Bachelerie F, Thomas D, Hay RT (1995) Inducible nuclear expression of newly synthesized I kappa B alpha negatively regulates DNA-binding and transcriptional activities of NF-kappa B. Mol Cell Biol 15: 2689-2696.
54. Ye RD (2001) Regulation of Nuclear factor kappa B activation by G-protein coupled receptors. J Leukoc Biol 70: 839-848.
55. 2+ in oxidant-induced NF-kappa B activation. FEBS 385: 58-62.
56. Mattson MP (1998) Free radicals, calcium, and the synaptic plasticity-cell death continuum: emerging roles of the transcription factor NF kappa B. Int Rev Neurobiol 42: 103-168.
57. Mattson MP, Meffert MK (2006) Roles for NF-kappa B in nerve cell survival, plasticity, and disease. Cell Death Differ 13: 852-860.
58. Camandola S, Mattson MP (2007) NF-kappa B as a therapeutic target in neurodegenerative diseases. Expert Opin Ther Targets 11: 123-132.
59. Hauser KF, Mangoura D (1998) Diversity of the endogenous opioid system in development: novel signal transduction translates multiple extracellular signals into neural cell growth and differentiation. Perspect Dev Neurobiol 5: 437-449.
60. Hauser KF, El-Hage N, Stiene-Martin A, Maragos WF, Nath A, et al. (2007) HIV-1 neuropathogenesis: glial mechanisms revealed through substance abuse. J Neurochem 100: 567-587.