Cooperative induction of CXCL10 involves NADPH oxidase: Implications for HIV dementia

GLIA

Volumn 58, Issue 5, 2010, Pages 611-621

  Williams, Rachel ^a   Yao, Honghong ^b   Peng, Fuwang ^b   Yang, Yanjing ^b   Bethel Brown, Crystal ^a   Buch, Shilpa ^a,b  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Astrocytes; CXCL10; HIV associated dementia; NADPH oxidase

Indexed keywords

APOCYNIN; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN KINASE B; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; TRANSACTIVATOR PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; ASTROCYTE; CONTROLLED STUDY; CYTOTOXICITY; DEMENTIA; ENZYME ACTIVATION; ENZYME INHIBITION; HIV ASSOCIATED DEMENTIA; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; NEUROTOXICITY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN TRANSPORT; RESPIRATORY BURST;

ACETOPHENONES; ASTROCYTES; CELL LINE, TRANSFORMED; CHEMOKINE CXCL10; DRUG INTERACTIONS; ENZYME INHIBITORS; ENZYME-LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; INTERFERON-ALPHA; INTERFERON-GAMMA; MEMBRANE GLYCOPROTEINS; NADPH OXIDASE; OXIDATIVE STRESS; PROTEIN TRANSPORT; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

EID: 77749339868     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20949     Document Type: Article

References (60)

1. Abramov AY, Duchen MR. 2005. The role of an astrocytic NADPH oxidase in the neurotoxicity of amyloid beta peptides. Philos Trans R Soc Lond B Biol Sci 360:2309-2314.
2. Abramov AY, Jacobson J, Wientjes F, Hothersall J, Canevari L, Duchen MR. 2005. Expression and modulation of an NADPH oxidase in mammalian astrocytes. J Neurosci 25:9176-9184.
3. Adachi T, Pimentel DR, Heibeck T, Hou X, Lee YJ, Jiang B, Ido Y, Cohen RA. 2004. S-glutathiolation of Ras mediates redox-sensitive signaling by angiotensin II in vascular smooth muscle cells. J Biol Chem 279:29857-29862.
4. Adler V, Yin Z, Tew KD, Ronai Z. 1999. Role of redox potential and reactive oxygen species in stress signaling. Oncogene 18:6104-6111.
5. Ahn JH, Lee M. 2008. Tyrosine phosphorylation and Ras activation is required for hydrogen peroxide-mediated Raf-1 kinase activation. Mol Cell Biochem 317:121-129.
6. Albright AV, Soldan SS, Gonzalez-Scarano F. 2003. Pathogenesis of human immunodeficiency virus-induced neurological disease. J Neurovirol 9:222-227.
7. Anrather J, Racchumi G, Iadecola C. 2006. NF-kappaB regulates phagocytic NADPH oxidase by inducing the expression of gp91phox. J Biol Chem 281:5657-5667.
8. Asensio VC, Maier J, Milner R, Boztug K, Kincaid C, Moulard M, Phillipson C, Lindsley K, Krucker T, Fox HS, Campbell IL. 2001. Interferon-independent, human immunodeficiency virus type 1 gp120-mediated induction of CXCL10/IP-10 gene expression by astrocytes in vivo and in vitro. J Virol 75:7067-7077.
9. Babior BM. 1999. NADPH oxidase: An update. Blood 93:1464-1476.
10. Basuroy S, Bhattacharya S, Leffler CW, Parfenova H. 2009. Nox4 NADPH oxidase mediates oxidative stress and apoptosis caused by TNF-α in cerebral vascular endothelial cells. Am J Physiol Cell Physiol 296:C422-C432.
11. Blokhina O, Virolainen E, Fagerstedt KV. 2003. Antioxidants, oxidative damage and oxygen deprivation stress: A review. Ann Bot 91:179-194.
12. Chanock SJ, el Benna J, Smith RM, Babior BM. 1994. The respiratory burst oxidase. J Biol Chem 269:24519-24522.
13. Davis RL, Syapin PJ. 2004. Chronic ethanol inhibits CXC chemokine ligand 10 production in human A172 astroglia and astroglial-mediated leukocyte chemotaxis. Neurosci Lett 362:220-225.
14. Davis RL, Dertien J, Syapin PJ. 2002. Ethanol-induced modulation of inducible nitric-oxide synthase activity in human A172 astrocytoma cells. Alcohol Clin Exp Res 26:1404-1411.
15. Dhillon N, Zhu X, Peng F, Yao H, Williams R, Callen S, Ladner AO, Buch S, Qiu J. 2008. Molecular mechanism(s) involved in the synergistic induction of CXCL10 by human immunodeficiency virus type 1 Tat and interferon-gamma in macrophages. J Neurovirol 14:196-204.
16. Dong Y, Benveniste EN. 2001. Immune function of astrocytes. Glia 36:180-190.
17. Dou H, Morehead J, Bradley J, Gorantla S, Ellison B, Kingsley J, Smith LM, Chao W, Bentsman G, Volsky DJ, et al. 2006. Neuropatho-logic and neuroinflammatory activities of HIV-1-infected human astrocytes in murine brain. Glia 54:81-93.
18. El-Benna J, Dang PM, Gougerot-Pocidalo MA, Elbim C. 2005. Phagocyte NADPH oxidase: A multicomponent enzyme essential for host defenses. Arch Immunol Ther Exp (Warsz) 53:199-206.
19. Firth CA, Yang YT, Gieseg SP. 2007. Lipid oxidation predominates over protein hydroperoxide formation in human monocyte-derived macrophages exposed to aqueous peroxyl radicals. Free Radic Res 41:839-848.
20. Ghosh S, Patel N, Rahn D, McAllister J, Sadeghi S, Horwitz G, Berry D, Wang KX, Swerdlow RH. 2007. The thiazolidinedione pioglitazone alters mitochondrial function in human neuron-like cells. Mol Pharmacol 71:1695-1702.
21. Giunta B, Obregon D, Hou H, Zeng J, Sun N, Nikolic V, Ehrhart J, Shytle D, Fernandez F, Tan J. 2006. EGCG mitigates neurotoxicity mediated by HIV-1 proteins gp120 and Tat in the presence of IFN-gamma: Role of JAK/STAT1 signaling and implications for HIV-associated dementia. Brain Res 1123:216-225.
22. Gonzalez-Scarano F, Martin-Garcia J. 2005. The neuropathogenesis of AIDS. Nat Rev Immunol 5:69-81.
23. Gorry PR, Ong C, Thorpe J, Bannwarth S, Thompson KA, Gatignol A, Vesselingh SL, Purcell DF. 2003. Astrocyte infection by HIV-1: Mechanisms of restricted virus replication, and role in the pathogenesis of HIV-1-associated dementia. Curr HIV Res 1:463-473.
24. Groemping Y, Rittinger K. 2005. Activation and assembly of the NADPH oxidase: A structural perspective. Biochem J 386 (Part 3):401-416.
25. Kaul M, Lipton SA. 2006. Mechanisms of neuronal injury and death in HIV-1 associated dementia. Curr HIV Res 4:307-318.
26. Kaul N, Forman HJ. 1996. Activation of NF kappa B by the respiratory burst of macrophages. Free Radic Biol Med 21:401-405.
27. Kolb SA, Sporer B, Lahrtz F, Koedel U, Pfister HW, Fontana A. 1999. Identification of a T cell chemotactic factor in the cerebrospinal fluid of HIV-1-infected individuals as interferon-gamma inducible protein 10. J Neuroimmunol 93:172-181.
28. Kolson DL, Pomerantz RJ. 1996. AIDS dementia and HIV-1-induced neurotoxicity: Possible pathogenic associations and mechanisms. J Biomed Sci 3:389-414.
29. Kuan YH, Lin RH, Chen YL, Tsao LT, Tzeng CC, Wang JP. 2006. Effective attenuation of acute lung injury in vivo and the formyl peptideinduced neutrophil activation in vitro by CYL-26z through the phosphoinositide 3-kinase gamma pathway. Biochem Pharmacol 72:749-760.
30. Kutsch O, Oh J, Nath A, Benveniste EN. 2000. Induction of the chemokines interleukin-8 and IP-10 by human immunodeficiency virus type 1 tat in astrocytes. J Virol 74:9214-9221.
31. 2-dependent recruitment of TRAF6 to endosomal interleukin-1 receptor complexes. Mol Cell Biol 26:140-154.
32. McArthur JC, Hoover DR, Bacellar H, Miller EN, Cohen BA, Becker JT, Graham NM, McArthur JH, Selnes OA, Jacobson LP, et al. 1993. Dementia in AIDS patients: Incidence and risk factors. Multicenter AIDS Cohort Study. Neurology 43:2245-2252.
33. Minagar A, Shapshak P, Fujimura R, Ownby R, Heyes M, Eisdorfer C. 2002. The role of macrophage/microglia and astrocytes in the pathogenesis of three neurologic disorders: HIV-associated dementia, Alzheimer disease, and multiple sclerosis J Neurol Sci 202:13-23.
34. Muscoli C, Salvemini D, Paolino D, Iannone M, Palma E, Cufari A, Rotiroti D, Perno CF, Aquaro S, Mollace V. 2002. Peroxynitrite decomposition catalyst prevents apoptotic cell death in a human astrocytoma cell line incubated with supernatants of HIV-infected macrophages. BMC Neurosci 3:13.
35. Nath A. 2002. Human immunodeficiency virus (HIV) proteins in neuropathogenesis of HIV dementia. J Infect Dis 186 (Suppl 2):S193-S198.
36. Navia BA, Cho ES, Petito CK, Price RW. 1986. The AIDS dementia complex: II. Neuropathology. Ann Neurol 19:525-535.
37. Ozdener H. 2005. Molecular mechanisms of HIV-1 associated neurodegeneration. J Biosci 30:391-405.
38. Park J, Choi K, Jeong E, Kwon D, Benveniste EN, Choi C. 2004. Reactive oxygen species mediate chloroquine-induced expression of chemokines by human astroglial cells. Glia 47:9-20.
39. Pocernich CB, Poon HF, Boyd-Kimball D, Lynn BC, Nath A, Klein JB, Butterfield DA. 2005a. Proteomic analysis of oxidatively modified proteins induced by the mitochondrial toxin 3-nitropropionic acid in human astrocytes expressing the HIV protein tat. Brain Res Mol Brain Res 133:299-306.
40. Pocernich CB, Sultana R, Mohmmad-Abdul H, Nath A, Butterfield DA. 2005b. HIV-dementia, Tat-induced oxidative stress, and antioxidant therapeutic considerations. Brain Res Brain Res Rev 50:14-26.
41. Quinn MT, Gauss KA. 2004. Structure and regulation of the neutrophil respiratory burst oxidase: Comparison with nonphagocyte oxidases. J Leukoc Biol 76:760-781.
42. Raad H, Paclet MH, Boussetta T, Kroviarski Y, Morel F, Quinn MT, Gougerot-Pocidalo MA, Dang PM, El-Benna J. 2008. Regulation of the phagocyte NADPH oxidase activity: Phosphorylation of gp91phox/ NOX2 by protein kinase C enhances its diaphorase activity and binding to Rac2, p67phox, and p47phox. FASEB J 23:1011-1022.
43. Saha RN, Pahan K. 2007. Differential regulation of Mn-superoxide dismutase in neurons and astroglia by HIV-1 gp120: Implications for HIV-associated dementia. Free Radic Biol Med 42:1866-1878.
44. Sanders VJ, Pittman CA, White MG, Wang G, Wiley CA, Achim CL. 1998. Chemokines and receptors in HIV encephalitis. Aids 12:1021-1026.
45. Song HY, Ryu J, Ju SM, Park LJ, Lee JA, Choi SY, Park J. 2007. Extracellular HIV-1 Tat enhances monocyte adhesion by up-regulation of ICAM-1 and VCAM-1 gene expression via ROS-dependent NF-kappaB activation in astrocytes. Exp Mol Med 39:27-37.
46. Stefanska J, Pawliczak R. 2008. Apocynin: Molecular aptitudes. Mediators Inflamm 2008:106507.
47. Sui Y, Potula R, Dhillon N, Pinson D, Li S, Nath A, Anderson C, Turchan J, Kolson D, Narayan O, et al. 2004. Neuronal apoptosis is mediated by CXCL10 overexpression in simian human immunodeficiency virus encephalitis. Am J Pathol 164:1557-1566.
48. Sui Y, Stehno-Bittel L, Li S, Loganathan R, Dhillon NK, Pinson D, Nath A, Kolson D, Narayan O, Buch S. 2006. CXCL10-induced cell death in neurons: Role of calcium dysregulation. Eur J Neurosci 23:957-964.
49. 2 for platelet-derived growth factor signal transduction. Science 270:296-299.
50. Thompson KA, McArthur JC, Wesselingh SL. 2001. Correlation between neurological progression and astrocyte apoptosis in HIV-associated dementia. Ann Neurol 49:745-752.
51. Turchan-Cholewo J, Dimayuga VM, Gupta S, Gorospe RM, Keller JN, Bruce-Keller AJ. 2009. NADPH oxidase drives cytokine and neurotoxin release from microglia and macrophages in response to HIV-Tat. Antioxid Redox Signal 11:193-204.
52. van Marle G, Henry S, Todoruk T, Sullivan A, Silva C, Rourke SB, Holden J, McArthur JC, Gill MJ, Power C. 2004. Human immunodeficiency virus type 1 Nef protein mediates neural cell death: A neurotoxic role for IP-10. Virology 329:302-318.
53. Vignais PV. 2002. The superoxide-generating NADPH oxidase: Structural aspects and activation mechanism. Cell Mol Life Sci 59:1428-1459.
54. Viviani B, Corsini E, Binaglia M, Galli CL, Marinovich M. 2001. Reactive oxygen species generated by glia are responsible for neuron death induced by human immunodeficiency virus-glycoprotein 120 in vitro. Neuroscience 107:51-58.
55. Wang X, Martindale JL, Liu Y, Holbrook NJ. 1998. The cellular response to oxidative stress: Influences of mitogen-activated protein kinase signalling pathways on cell survival. Biochem J 333 (Part 2):291-300.
56. Wang Z, Trillo-Pazos G, Kim SY, Canki M, Morgello S, Sharer LR, Gelbard HA, Su ZZ, Kang DC, Brooks AI, et al. 2004. Effects of human immunodeficiency virus type 1 on astrocyte gene expression and function: Potential role in neuropathogenesis. J Neurovirol 10 (Suppl 1):25-32.
57. Williams R, Dhillon NK, Hegde ST, Yao H, Peng F, Callen S, Chebloune Y, Davis RL, Buch SJ. 2008. Proinflammatory cytokines and HIV-1 synergistically enhance CXCL10 expression in human astrocytes. Glia 57:734-743.
58. Williams R Yao H, Dhillon NK, Buch SJ. 2009. HIV-1 Tat co-operates with IFN-γ and TNF-α to increase CXCL10 in human astrocytes. PLoS One 4:e5709.
59. Yao HH, Ding JH, Zhou F, Wang F, Hu LF, Sun T, Hu G. 2005. Enhancement of glutamate uptake mediates the neuroprotection exerted by activating group II or III metabotropic glutamate receptors on astrocytes. J Neurochem 92:948-961.
60. Yao H, Peng F, Dhillon N, Callen S, Bokhari S, Stehno-Bittel L, Ahmad SO, Wang JQ, Buch S. 2009. Involvement of TRPC channels in CCL2-mediated neuroprotection against tat toxicity. J Neurosci 29:1657-1669.