Human immunodeficiency virus type 1 viral protein R (Vpr) induces CCL5 expression in astrocytes via PI3K and MAPK signaling pathways

Journal of Neuroinflammation

Volumn 10, Issue , 2013, Pages

  Gangwani, Mohitkumar R ^a   Noel, Richard J ^b   Shah, Ankit ^a   Rivera Amill, Vanessa ^b   Kumar, Anil ^a  

^a UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

^b PONCE SCHOOL OF MEDICINE   (Puerto Rico)

Author keywords

AP 1; CCL5; HIV 1; MAPK; NF kB; PI3K Akt; Vpr

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN AKT 3; PROTEIN INHIBITOR; PROTEIN KINASE B; PROTEIN KINASE B BETA; PROTEIN P50; RANTES; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG; VPR PROTEIN;

ARTICLE; ASTROCYTE; BIOACCUMULATION; CELL STRAIN; CELL STRAIN SVGA; CONTROLLED STUDY; CYTOKINE PRODUCTION; FETUS; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PLASMID; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; VIRUS CELL INTERACTION;

ASTROCYTES; CELL LINE; CHEMOKINE CCL5; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; PHOSPHATIDYLINOSITOL 3-KINASES; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSFECTION; VPR GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

EID: 84887332032     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-10-136     Document Type: Article

References (57)

1. Koenig S, Gendelman HE, Orenstein JM, Dal Canto MC, Pezeshkpour GH, Yungbluth M, Janotta F, Aksamit A, Martin MA, Fauci AS. Detection of AIDS virus in macrophages in brain tissue from AIDS patients with encephalopathy. Science 1986, 233(4768):1089-1093. 10.1126/science.3016903, 3016903.
2. Vazeux R, Brousse N, Jarry A, Henin D, Marche C, Vedrenne C, Mikol J, Wolff M, Michon C, Rozenbaum W, et al. AIDS subacute encephalitis. identification of HIV-infected cells. Am J Pathol 1987, 126(3):403-410. 1899654, 3548405.
3. Valcour V, Chalermchai T, Sailasuta N, Marovich M, Lerdlum S, Suttichom D, Suwanwela NC, Jagodzinski L, Michael N, Spudich S, et al. Central nervous system viral invasion and inflammation during acute HIV infection. J Infect Dis 2012, 206(2):275-282. 10.1093/infdis/jis326, 3490695, 22551810.
4. Heaton RK, Clifford DB, Franklin DR, Woods SP, Ake C, Vaida F, Ellis RJ, Letendre SL, Marcotte TD, Atkinson JH, et al. HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy: CHARTER Study. Neurology 2010, 75(23):2087-2096. 10.1212/WNL.0b013e318200d727, 2995535, 21135382.
5. Adle-Biassette H, Chretien F, Wingertsmann L, Hery C, Ereau T, Scaravilli F, Tardieu M, Gray F. Neuronal apoptosis does not correlate with dementia in HIV infection but is related to microglial activation and axonal damage. Neuropathol Appl Neurobiol 1999, 25(2):123-133. 10.1046/j.1365-2990.1999.00167.x, 10216000.
6. Glass JD, Fedor H, Wesselingh SL, McArthur JC. Immunocytochemical quantitation of human immunodeficiency virus in the brain: correlations with dementia. Ann Neurol 1995, 38(5):755-762. 10.1002/ana.410380510, 7486867.
7. Ricci G, Volpi L, Pasquali L, Petrozzi L, Siciliano G. Astrocyte-neuron interactions in neurological disorders. J Biol Phys 2009, 35(4):317-336. 10.1007/s10867-009-9157-9, 2750745, 19669420.
8. Li J, Bentsman G, Potash MJ, Volsky DJ. Human immunodeficiency virus type 1 efficiently binds to human fetal astrocytes and induces neuroinflammatory responses independent of infection. BMC Neurosci 2007, 8:31. 10.1186/1471-2202-8-31, 1884168, 17498309.
9. Carroll-Anzinger D, Al-Harthi L. Gamma interferon primes productive human immunodeficiency virus infection in astrocytes. J Virol 2006, 80(1):541-544. 10.1128/JVI.80.1.541-544.2006, 1317538, 16352578.
10. Hori K, Burd PR, Furuke K, Kutza J, Weih KA, Clouse KA. Human immunodeficiency virus-1-infected macrophages induce inducible nitric oxide synthase and nitric oxide (NO) production in astrocytes: astrocytic NO as a possible mediator of neural damage in acquired immunodeficiency syndrome. Blood 1999, 93(6):1843-1850.
11. Grimaldi LM, Martino GV, Franciotta DM, Brustia R, Castagna A, Pristera R, Lazzarin A. Elevated alpha-tumor necrosis factor levels in spinal fluid from HIV-1-infected patients with central nervous system involvement. Ann Neurol 1991, 29(1):21-25. 10.1002/ana.410290106, 1996875.
12. Heyes MP, Brew BJ, Martin A, Price RW, Salazar AM, Sidtis JJ, Yergey JA, Mouradian MM, Sadler AE, Keilp J, et al. Quinolinic acid in cerebrospinal fluid and serum in HIV-1 infection: relationship to clinical and neurological status. Ann Neurol 1991, 29(2):202-209. 10.1002/ana.410290215, 1826418.
13. Kelder W, McArthur JC, Nance-Sproson T, McClernon D, Griffin DE. Beta-chemokines MCP-1 and RANTES are selectively increased in cerebrospinal fluid of patients with human immunodeficiency virus-associated dementia. Ann Neurol 1998, 44(5):831-835. 10.1002/ana.410440521, 9818943.
14. Kutsch O, Oh J, Nath A, Benveniste EN. Induction of the chemokines interleukin-8 and IP-10 by human immunodeficiency virus type 1 tat in astrocytes. J Virol 2000, 74(19):9214-9221. 10.1128/JVI.74.19.9214-9221.2000, 102120, 10982368.
15. Wahl SM, Allen JB, McCartney-Francis N, Morganti-Kossmann MC, Kossmann T, Ellingsworth L, Mai UE, Mergenhagen SE, Orenstein JM. Macrophage- and astrocyte-derived transforming growth factor beta as a mediator of central nervous system dysfunction in acquired immune deficiency syndrome. J Exp Med 1991, 173(4):981-991. 10.1084/jem.173.4.981, 2190818, 2007861.
16. Hesselgesser J, Taub D, Baskar P, Greenberg M, Hoxie J, Kolson DL, Horuk R. Neuronal apoptosis induced by HIV-1 gp120 and the chemokine SDF-1 alpha is mediated by the chemokine receptor CXCR4. Curr Biol 1998, 8(10):595-598. 10.1016/S0960-9822(98)70230-1, 9601645.
17. Haughey NJ, Mattson MP. Calcium dysregulation and neuronal apoptosis by the HIV-1 proteins Tat and gp120. J Acquir Immune Defic Syndr 2002, 31(Suppl 2):S55-S61.
18. Shah A, Kumar A. HIV-1 gp120-mediated increases in IL-8 production in astrocytes are mediated through the NF-kappaB pathway and can be silenced by gp120-specific siRNA. J Neuroinflammation 2010, 7:96. 10.1186/1742-2094-7-96, 3023744, 21190575.
19. Shah A, Singh DP, Buch S, Kumar A. HIV-1 envelope protein gp120 up regulates CCL5 production in astrocytes which can be circumvented by inhibitors of NF-kappaB pathway. Biochem Biophys Res Commun 2011, 414(1):112-117. 10.1016/j.bbrc.2011.09.033, 3204359, 21945445.
20. Shah A, Verma AS, Patel KH, Noel R, Rivera-Amill V, Silverstein PS, Chaudhary S, Bhat HK, Stamatatos L, Singh DP, et al. HIV-1 gp120 induces expression of IL-6 through a nuclear factor-kappa B-dependent mechanism: suppression by gp120 specific small interfering RNA. PLoS One 2011, 6(6):e21261. 10.1371/journal.pone.0021261, 3119684, 21712995.
21. He J, Choe S, Walker R, Di Marzio P, Morgan DO, Landau NR. Human immunodeficiency virus type 1 viral protein R (Vpr) arrests cells in the G2 phase of the cell cycle by inhibiting p34cdc2 activity. J Virol 1995, 69(11):6705-6711. 189580, 7474080.
22. Heinzinger NK, Bukinsky MI, Haggerty SA, Ragland AM, Kewalramani V, Lee MA, Gendelman HE, Ratner L, Stevenson M, Emerman M. The Vpr protein of human immunodeficiency virus type 1 influences nuclear localization of viral nucleic acids in nondividing host cells. Proc Natl Acad Sci USA 1994, 91(15):7311-7315. 10.1073/pnas.91.15.7311, 44389, 8041786.
23. Vanitharani R, Mahalingam S, Rafaeli Y, Singh SP, Srinivasan A, Weiner DB, Ayyavoo V. HIV-1 Vpr transactivates LTR-directed expression through sequences present within -278 to -176 and increases virus replication in vitro. Virology 2001, 289(2):334-342. 10.1006/viro.2001.1153, 11689055.
24. Ayyavoo V, Mahalingam S, Rafaeli Y, Kudchodkar S, Chang D, Nagashunmugam T, Williams WV, Weiner DB. HIV-1 viral protein R (Vpr) regulates viral replication and cellular proliferation in T cells and monocytoid cells in vitro. Journal of leukocyte biology 1997, 62(1):93-99.
25. Levy DN, Refaeli Y, Weiner DB. Extracellular Vpr protein increases cellular permissiveness to human immunodeficiency virus replication and reactivates virus from latency. Journal of virology 1995, 69(2):1243-1252. 188697, 7815499.
26. Mukerjee R, Chang JR, Del Valle L, Bagashev A, Gayed MM, Lyde RB, Hawkins BJ, Brailoiu E, Cohen E, Power C, et al. Deregulation of microRNAs by HIV-1 Vpr protein leads to the development of neurocognitive disorders. J Biol Chem 2011, 286(40):34976-34985. 10.1074/jbc.M111.241547, 3186354, 21816823.
27. Jones GJ, Barsby NL, Cohen EA, Holden J, Harris K, Dickie P, Jhamandas J, Power C. HIV-1 Vpr causes neuronal apoptosis and in vivo neurodegeneration. J Neurosci 2007, 27(14):3703-3711. 10.1523/JNEUROSCI.5522-06.2007, 17409234.
28. Rom I, Deshmane SL, Mukerjee R, Khalili K, Amini S, Sawaya BE. HIV-1 Vpr deregulates calcium secretion in neural cells. Brain Res 2009, 1275:81-86. 2692350, 19328187.
29. Kitayama H, Miura Y, Ando Y, Hoshino S, Ishizaka Y, Koyanagi Y. Human immunodeficiency virus type 1 Vpr inhibits axonal outgrowth through induction of mitochondrial dysfunction. J Virol 2008, 82(5):2528-2542. 10.1128/JVI.02094-07, 2258941, 18094160.
30. Hoshino S, Konishi M, Mori M, Shimura M, Nishitani C, Kuroki Y, Koyanagi Y, Kano S, Itabe H, Ishizaka Y. HIV-1 Vpr induces TLR4/MyD88-mediated IL-6 production and reactivates viral production from latency. J Leukoc Biol 2010, 87(6):1133-1143. 10.1189/jlb.0809547, 20145198.
31. Si Q, Kim MO, Zhao ML, Landau NR, Goldstein H, Lee S. Vpr- and Nef-dependent induction of RANTES/CCL5 in microglial cells. Virology 2002, 301(2):342-353. 10.1006/viro.2002.1613, 12359436.
32. Major EO, Miller AE, Mourrain P, Traub RG, de Widt E, Sever J. Establishment of a line of human fetal glial cells that supports JC virus multiplication. Proc Natl Acad Sci USA 1985, 82(4):1257-1261. 10.1073/pnas.82.4.1257, 397234, 2983332.
33. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008, 3(6):1101-1108. 10.1038/nprot.2008.73, 18546601.
34. Uddin S, Ah-Kang J, Ulaszek J, Mahmud D, Wickrema A. Differentiation stage-specific activation of p38 mitogen-activated protein kinase isoforms in primary human erythroid cells. Proc Natl Acad Sci USA 2004, 101(1):147-152. 10.1073/pnas.0307075101, 314153, 14694199.
35. Fillmore GC, Wang Q, Carey MJ, Kim CH, Elenitoba-Johnson KS, Lim MS. Expression of Akt (protein kinase B) and its isoforms in malignant lymphomas. Leuk Lymphoma 2005, 46(12):1765-1773. 10.1080/10428190500159944, 16263580.
36. Lee JC, Kassis S, Kumar S, Badger A, Adams JL. p38 mitogen-activated protein kinase inhibitors-mechanisms and therapeutic potentials. Pharmacol Ther 1999, 82(2-3):389-397.
37. Muthumani K, Hwang DS, Desai BM, Zhang D, Dayes N, Green DR, Weiner DB. HIV-1 Vpr induces apoptosis through caspase 9 in T cells and peripheral blood mononuclear cells. J Biol Chem 2002, 277(40):37820-37831. 10.1074/jbc.M205313200, 12095993.
38. Patel CA, Mukhtar M, Pomerantz RJ. Human immunodeficiency virus type 1 Vpr induces apoptosis in human neuronal cells. J Virol 2000, 74(20):9717-9726. 10.1128/JVI.74.20.9717-9726.2000, 112404, 11000244.
39. Noorbakhsh F, Ramachandran R, Barsby N, Ellestad KK, LeBlanc A, Dickie P, Baker G, Hollenberg MD, Cohen EA, Power C. MicroRNA profiling reveals new aspects of HIV neurodegeneration: caspase-6 regulates astrocyte survival. FASEB J 2010, 24(6):1799-1812. 10.1096/fj.09-147819, 20097875.
40. Roux P, Alfieri C, Hrimech M, Cohen EA, Tanner JE. Activation of transcription factors NF-kappaB and NF-IL-6 by human immunodeficiency virus type 1 protein R (Vpr) induces interleukin-8 expression. J Virol 2000, 74(10):4658-4665. 10.1128/JVI.74.10.4658-4665.2000, 111986, 10775602.
41. Gordon CJ, Muesing MA, Proudfoot AE, Power CA, Moore JP, Trkola A. Enhancement of human immunodeficiency virus type 1 infection by the CC-chemokine RANTES is independent of the mechanism of virus-cell fusion. J Virol 1999, 73(1):684-694. 103875, 9847374.
42. Meucci O, Fatatis A, Simen AA, Bushell TJ, Gray PW, Miller RJ. Chemokines regulate hippocampal neuronal signaling and gp120 neurotoxicity. Proc Natl Acad Sci USA 1998, 95(24):14500-14505. 10.1073/pnas.95.24.14500, 24402, 9826729.
43. Kaul M, Lipton SA. Chemokines and activated macrophages in HIV gp120-induced neuronal apoptosis. Proc Natl Acad Sci USA 1999, 96(14):8212-8216. 10.1073/pnas.96.14.8212, 22214, 10393974.
44. Valerio A, Ferrario M, Martinez FO, Locati M, Ghisi V, Bresciani LG, Mantovani A, Spano P. Gene expression profile activated by the chemokine CCL5/RANTES in human neuronal cells. J Neurosci Res 2004, 78(3):371-382. 10.1002/jnr.20250, 15389840.
45. Cartier L, Dubois-Dauphin M, Hartley O, Irminger-Finger I, Krause KH. Chemokine-induced cell death in CCR5-expressing neuroblastoma cells. J Neuroimmunol 2003, 145(1-2):27-39.
46. Catalfamo M, Karpova T, McNally J, Costes SV, Lockett SJ, Bos E, Peters PJ, Henkart PA. Human CD8+ T cells store RANTES in a unique secretory compartment and release it rapidly after TcR stimulation. Immunity 2004, 20(2):219-230. 10.1016/S1074-7613(04)00027-5, 14975243.
47. Wickremasinghe MI, Thomas LH, O'Kane CM, Uddin J, Friedland JS. Transcriptional mechanisms regulating alveolar epithelial cell-specific CCL5 secretion in pulmonary tuberculosis. J Biol Chem 2004, 279(26):27199-27210. 10.1074/jbc.M403107200, 15117956.
48. Kishore N, Sommers C, Mathialagan S, Guzova J, Yao M, Hauser S, Huynh K, Bonar S, Mielke C, Albee L, et al. A selective IKK-2 inhibitor blocks NF-kappa B-dependent gene expression in interleukin-1 beta-stimulated synovial fibroblasts. J Biol Chem 2003, 278(35):32861-32871. 10.1074/jbc.M211439200, 12813046.
49. Oeckinghaus A, Hayden MS, Ghosh S. Crosstalk in NF-kappaB signaling pathways. Nat Immunol 2011, 12(8):695-708. 10.1038/ni.2065, 21772278.
50. Lin MS, Hung KS, Chiu WT, Sun YY, Tsai SH, Lin JW, Lee YH. Curcumin enhances neuronal survival in N-methyl-d-aspartic acid toxicity by inducing RANTES expression in astrocytes via PI-3 K and MAPK signaling pathways. Prog Neuropsychopharmacol Biol Psychiatry 2011, 35(4):931-938. 10.1016/j.pnpbp.2010.12.022, 21199667.
51. Casola A, Garofalo RP, Haeberle H, Elliott TF, Lin R, Jamaluddin M, Brasier AR. Multiple cis regulatory elements control RANTES promoter activity in alveolar epithelial cells infected with respiratory syncytial virus. J Virol 2001, 75(14):6428-6439. 10.1128/JVI.75.14.6428-6439.2001, 114366, 11413310.
52. Santi SA, Lee H. The Akt isoforms are present at distinct subcellular locations. Am J Physiol Cell Physiol 2010, 298(3):C580-C591. 10.1152/ajpcell.00375.2009, 20018949.
53. Easton RM, Cho H, Roovers K, Shineman DW, Mizrahi M, Forman MS, Lee VM, Szabolcs M, de Jong R, Oltersdorf T, et al. Role for Akt3/protein kinase Bgamma in attainment of normal brain size. Mol Cell Biol 2005, 25(5):1869-1878. 10.1128/MCB.25.5.1869-1878.2005, 549378, 15713641.
54. Tsiperson V, Gruber RC, Goldberg MF, Jordan A, Weinger JG, Macian F, Shafit-Zagardo B. Suppression of inflammatory responses during myelin oligodendrocyte glycoprotein-induced experimental autoimmune encephalomyelitis is regulated by AKT3 signaling. J Immunol 2013, 190(4):1528-1539. 10.4049/jimmunol.1201387, 23335751.
55. Arranz A, Doxaki C, Vergadi E, de la Torre MY, Vaporidi K, Lagoudaki ED, Ieronymaki E, Androulidaki A, Venihaki M, Margioris AN, et al. Akt1 and Akt2 protein kinases differentially contribute to macrophage polarization. Proc Natl Acad Sci USA 2012, 109(24):9517-9522. 10.1073/pnas.1119038109, 3386059, 22647600.
56. Eckert RL, Adhikary G, Young CA, Jans R, Crish JF, Xu W, Rorke EA. AP1 transcription factors in epidermal differentiation and skin cancer. J Skin Cancer 2013, 2013:537028. 3676924, 23762562.
57. Varin A, Decrion AZ, Sabbah E, Quivy V, Sire J, Van Lint C, Roques BP, Aggarwal BB, Herbein G. Synthetic Vpr protein activates activator protein-1, c-Jun N-terminal kinase, and NF-kappaB and stimulates HIV-1 transcription in promonocytic cells and primary macrophages. J Biol Chem 2005, 280(52):42557-42567. 10.1074/jbc.M502211200, 16243842.