HIV-1 Tat Protein Increases Microglial Outward K+ Current and Resultant Neurotoxic Activity

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Liu, Jianuo ^a   Xu, Peng ^a   Collins, Cory ^a   Liu, Han ^a   Zhang, Jingdong ^a   Keblesh, James P ^a   Xiong, Huangui ^a,b  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1BETA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NITRIC OXIDE; POTASSIUM CHANNEL BLOCKING AGENT; POTASSIUM CHANNEL KV1.3; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; TRANSACTIVATOR PROTEIN; TUMOR NECROSIS FACTOR ALPHA; VIRUS RNA;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN PROTECTION; CELL ACTIVATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; ENZYME REPRESSION; HUMAN IMMUNODEFICIENCY VIRUS 1; INTRACELLULAR SIGNALING; MICROGLIA; NERVE CELL; NEUROTOXICITY; NEWBORN; NONHUMAN; POTASSIUM CURRENT; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; RAT;

ANIMALS; ELECTROPHYSIOLOGICAL PROCESSES; GENE KNOCKDOWN TECHNIQUES; HIV-1; KV1.3 POTASSIUM CHANNEL; MAP KINASE SIGNALING SYSTEM; MICROGLIA; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEURONS; NEUROTOXINS; POTASSIUM; POTASSIUM CHANNEL BLOCKERS; RATS; RATS, SPRAGUE-DAWLEY; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; UP-REGULATION;

HUMAN IMMUNODEFICIENCY VIRUS 1; RATTUS;

EID: 84878518887     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064904     Document Type: Article

References (61)

1. Kaul M, Lipton SA, (2006) Mechanisms of neuronal injury and death in HIV-1 associated dementia. Curr HIV Res 4: 307-318.
2. Antinori A, Arendt G, Becker JT, Brew BJ, Byrd DA, et al. (2007) Updated research nosology for HIV-associated neurocognitive disorders. Neurology 69: 1789-1799.
3. Robertson KR, Smurzynski M, Parsons TD, Wu K, Bosch RJ, et al. (2007) The prevalence and incidence of neurocognitive impairment in the HAART era. AIDS 21: 1915-1921.
4. Heaton RK, Clifford DB, Franklin DR Jr, Woods SP, Ake C, et al. (2010) HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy: CHARTER Study. Neurology 75: 2087-2096.
5. Spudich SS, Ances BM, (2011) Central nervous system complications of HIV infection. Top Antivir Med 19: 48-57.
6. Glass JD, Fedor H, Wesselingh SL, McArthur JC, (1995) Immunocytochemical quantitation of human immunodeficiency virus in the brain: correlations with dementia. Ann Neurol 38: 755-762.
7. Gendelman HE, Eiden L, Epstein L, Grant I, Lipton S, et al. (1998) The Neuropathogenesis of HIV-1-Dementia: APanel Discussion. In: Gendelman HE, Lipton SA, Epstein LG, Swindells S, editors. The neurology of AIDS. 1 ed. New York: Chapman and Hall. pp. 1-10.
8. Garden GA, (2002) Microglia in human immunodeficiency virus-associated neurodegeneration. Glia 40: 240-251.
9. Kielian T, (2004) Microglia and chemokines in infectious diseases of the nervous system: views and reviews. Front Biosci 9: 732-750.
10. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A, (2011) Physiology of microglia. Physiol Rev 91: 461-553.
11. Wickenden A, (2002) K(+) channels as therapeutic drug targets. Pharmacol Ther 94: 157-182.
12. Judge SI, Lee JM, Bever CT Jr, Hoffman PM, (2006) Voltage-gated potassium channels in multiple sclerosis: Overview and new implications for treatment of central nervous system inflammation and degeneration. J Rehabil Res Dev 43: 111-122.
13. Norenberg W, Gebicke-Haerter PJ, Illes P, (1994) Voltage-dependent potassium channels in activated rat microglia. J Physiol 475: 15-32.
14. Fischer HG, Eder C, Hadding U, Heinemann U, (1995) Cytokine-dependent K+ channel profile of microglia at immunologically defined functional states. Neuroscience 64: 183-191.
15. Eder C, (1998) Ion channels in microglia (brain macrophages). Am J Physiol 275: C327-342.
16. Schilling T, Quandt FN, Cherny VV, Zhou W, Heinemann U, et al. (2000) Upregulation of Kv1.3 K(+) channels in microglia deactivated by TGF-beta. Am J Physiol Cell Physiol 279: C1123-1134.
17. Kettenmann H, Hoppe D, Gottmann K, Banati R, Kreutzberg G, (1990) Cultured microglial cells have a distinct pattern of membrane channels different from peritoneal macrophages. J Neurosci Res 26: 278-287.
18. Eder C, Schilling T, Heinemann U, Haas D, Hailer N, et al. (1999) Morphological, immunophenotypical and electrophysiological properties of resting microglia in vitro. Eur J Neurosci 11: 4251-4261.
19. Walz W, Bekar LK, (2001) Ion channels in cultured microglia. Microsc Res Tech 54: 26-33.
20. Farber K, Kettenmann H, (2005) Physiology of microglial cells. Brain Res Brain Res Rev 48: 133-143.
21. Gendelman HE, Ding S, Gong N, Liu J, Ramirez SH, et al. (2009) Monocyte chemotactic protein-1 regulates voltage-gated K+ channels and macrophage transmigration. J Neuroimmune Pharmacol 4: 47-59.
22. Fordyce CB, Jagasia R, Zhu X, Schlichter LC, (2005) Microglia Kv1.3 channels contribute to their ability to kill neurons. J Neurosci 25: 7139-7149.
23. Nutile-McMenemy N, Elfenbein A, Deleo JA, (2007) Minocycline decreases in vitro microglial motility, beta1-integrin, and Kv1.3 channel expression. J Neurochem 103: 2035-2046.
24. Liu J, Xu C, Chen L, Xu P, Xiong H, (2012) Involvement of Kv1.3 and p38 MAPK signaling in HIV-1 glycoprotein 120-induced microglia neurotoxicity. Cell Death Dis 3: e254.
25. Xu C, Liu J, Chen L, Liang S, Fujii N, et al. (2011) HIV-1 gp120 enhances outward potassium current via CXCR4 and cAMP-dependent protein kinase A signaling in cultured rat microglia. Glia 59: 997-1007.
26. Westendorp MO, Frank R, Ochsenbauer C, Stricker K, Dhein J, et al. (1995) Sensitization of T cells to CD95-mediated apoptosis by HIV-1 Tat and gp120. Nature 375: 497-500.
27. Xiao H, Neuveut C, Tiffany HL, Benkirane M, Rich EA, et al. (2000) Selective CXCR4 antagonism by Tat: implications for in vivo expansion of coreceptor use by HIV-1. Proc Natl Acad Sci U S A 97: 11466-11471.
28. Bonavia R, Bajetto A, Barbero S, Albini A, Noonan DM, et al. (2001) HIV-1 Tat causes apoptotic death and calcium homeostasis alterations in rat neurons. Biochem Biophys Res Commun 288: 301-308.
29. Hayashi K, Pu H, Andras IE, Eum SY, Yamauchi A, et al. (2006) HIV-TAT protein upregulates expression of multidrug resistance protein 1 in the blood-brain barrier. J Cereb Blood Flow Metab 26: 1052-1065.
30. Koistinaho M, Koistinaho J, (2002) Role of p38 and p44/42 mitogen-activated protein kinases in microglia. Glia 40: 175-183.
31. Strniskova M, Barancik M, Ravingerova T, (2002) Mitogen-activated protein kinases and their role in regulation of cellular processes. Gen Physiol Biophys 21: 231-255.
32. Kaminska B, Gozdz A, Zawadzka M, Ellert-Miklaszewska A, Lipko M, (2009) MAPK signal transduction underlying brain inflammation and gliosis as therapeutic target. Anat Rec (Hoboken) 292: 1902-1913.
33. Koenig S, Gendelman HE, Orenstein JM, Dal Canto MC, Pezeshkpour GH, et al. (1986) Detection of AIDS virus in macrophages in brain tissue from AIDS patients with encephalopathy. Science 233: 1089-1093.
34. Genis P, Jett M, Bernton EW, Boyle T, Gelbard HA, et al. (1992) Cytokines and arachidonic metabolites produced during human immunodeficiency virus (HIV)-infected macrophage-astroglia interactions: implications for the neuropathogenesis of HIV disease. J Exp Med 176: 1703-1718.
35. Kaul M, Garden GA, Lipton SA, (2001) Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature 410: 988-994.
36. Menteyne A, Levavasseur F, Audinat E, Avignone E, (2009) Predominant functional expression of Kv1.3 by activated microglia of the hippocampus after Status epilepticus. PLoS One 4: e6770.
37. Alizadeh AA, Eisen MB, Davis RE, Ma C, Lossos IS, et al. (2000) Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 403: 503-511.
38. Abdul M, Santo A, Hoosein N, (2003) Activity of potassium channel-blockers in breast cancer. Anticancer Res 23: 3347-3351.
39. Brevet M, Ahidouch A, Sevestre H, Merviel P, El Hiani Y, et al. (2008) Expression of K+ channels in normal and cancerous human breast. Histol Histopathol 23: 965-972.
40. Schilling T, Eder C, (2011) Amyloid-beta-induced reactive oxygen species production and priming are differentially regulated by ion channels in microglia. J Cell Physiol 226: 3295-3302.
41. Kramer-Hammerle S, Rothenaigner I, Wolff H, Bell JE, Brack-Werner R, (2005) Cells of the central nervous system as targets and reservoirs of the human immunodeficiency virus. Virus Res 111: 194-213.
42. Hanisch UK, (2002) Microglia as a source and target of cytokines. Glia 40: 140-155.
43. Kim SU, de Vellis J, (2005) Microglia in health and disease. J Neurosci Res 81: 302-313.
44. Dheen ST, Kaur C, Ling EA, (2007) Microglial activation and its implications in the brain diseases. Curr Med Chem 14: 1189-1197.
45. Lee YB, Schrader JW, Kim SU, (2000) p38 map kinase regulates TNF-alpha production in human astrocytes and microglia by multiple mechanisms. Cytokine 12: 874-880.
46. Nagata Y, Todokoro K, (1999) Requirement of activation of JNK and p38 for environmental stress-induced erythroid differentiation and apoptosis and of inhibition of ERK for apoptosis. Blood 94: 853-863.
47. Lokensgard JR, Hu S, Hegg CC, Thayer SA, Gekker G, et al. (2001) Diazepam inhibits HIV-1 Tat-induced migration of human microglia. J Neurovirol 7: 481-486.
48. Eugenin EA, Dyer G, Calderon TM, Berman JW, (2005) HIV-1 tat protein induces a migratory phenotype in human fetal microglia by a CCL2 (MCP-1)-dependent mechanism: possible role in NeuroAIDS. Glia 49: 501-510.
49. Visentin S, Renzi M, Levi G, (2001) Altered outward-rectifying K(+) current reveals microglial activation induced by HIV-1 Tat protein. Glia 33: 181-190.
50. Keblesh JP, Dou H, Gendelman HE, Xiong H, (2009) 4-Aminopyridine improves spatial memory in a murine model of HIV-1 encephalitis. J Neuroimmune Pharmacol 4: 317-327.
51. Chandy KG, Wulff H, Beeton C, Pennington M, Gutman GA, et al. (2004) K+ channels as targets for specific immunomodulation. Trends Pharmacol Sci 25: 280-289.
52. Beeton C, Wulff H, Standifer NE, Azam P, Mullen KM, et al. (2006) Kv1.3 channels are a therapeutic target for T cell-mediated autoimmune diseases. Proc Natl Acad Sci U S A 103: 17414-17419.
53. Chandy KG, DeCoursey TE, Cahalan MD, McLaughlin C, Gupta S, (1984) Voltage-gated potassium channels are required for human T lymphocyte activation. J Exp Med 160: 369-385.
54. Wulff H, Beeton C, Chandy KG, (2003) Potassium channels as therapeutic targets for autoimmune disorders. Curr Opin Drug Discov Devel 6: 640-647.
55. Beeton C, Wulff H, Singh S, Botsko S, Crossley G, et al. (2003) A novel fluorescent toxin to detect and investigate Kv1.3 channel up-regulation in chronically activated T lymphocytes. J Biol Chem 278: 9928-9937.
56. Wulff H, Calabresi PA, Allie R, Yun S, Pennington M, et al. (2003) The voltage-gated Kv1.3 K(+) channel in effector memory T cells as new target for MS. J Clin Invest 111: 1703-1713.
57. Vianna-Jorge R, Suarez-Kurtz G, (2004) Potassium channels in T lymphocytes: therapeutic targets for autoimmune disorders? BioDrugs 18: 329-341.
58. Beeton C, Pennington MW, Norton RS, (2011) Analogs of the sea anemone potassium channel blocker ShK for the treatment of autoimmune diseases. Inflamm Allergy Drug Targets 10: 313-321.
59. Valverde P, Kawai T, Taubman MA, (2005) Potassium channel-blockers as therapeutic agents to interfere with bone resorption of periodontal disease. J Dent Res 84: 488-499.
60. Goffe B, Papp K, Gratton D, Krueger GG, Darif M, et al. (2005) An integrated analysis of thirteen trials summarizing the long-term safety of alefacept in psoriasis patients who have received up to nine courses of therapy. Clin Ther 27: 1912-1921.
61. Esamai F, Tenge CN, Ayuo PO, Ong'or WO, Obala A, et al. (2005) A randomized open label clinical trial to compare the efficacy and safety of intravenous quinine followed by oral malarone vs. intravenous quinine followed by oral quinine in the treatment of severe malaria. J Trop Pediatr 51: 17-24.