HIV-1 Viral Protein R Activates NLRP3 Inflammasome in Microglia: implications for HIV-1 Associated Neuroinflammation

Journal of Neuroimmune Pharmacology

Volumn 12, Issue 2, 2017, Pages 233-248

  Mamik, Manmeet K ^a   Hui, Elizabeth ^a   Branton, William G ^a   McKenzie, Brienne A ^a   Chisholm, Jesse ^a   Cohen, Eric A ^b   Power, Christopher ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

Author keywords

HIV 1; Inflammasomes; Interleukin 1 beta; Neuroinflammation; NLRP3; Viral protein R

Indexed keywords

BELNACASAN; CRYOPYRIN; GAG PROTEIN; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; TUMOR NECROSIS FACTOR; VPR PROTEIN; AUTACOID; NLRP3 PROTEIN, HUMAN;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CELL ACTIVATION; CELL VIABILITY; CEREBROSPINAL FLUID ANALYSIS; COGNITION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FETUS; GENE ACTIVATION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IMMUNOSTIMULATION; MACROPHAGE; MALE; MICROGLIA; MIDDLE AGED; MOUSE; NERVOUS SYSTEM INFLAMMATION; NEUROPSYCHIATRY; NONHUMAN; OPEN FIELD BEHAVIOR; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEROCONVERSION; VERY ELDERLY; ANIMAL; CELL CULTURE; CELL SURVIVAL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; INFLAMMATION; METABOLISM; PHYSIOLOGY; TRANSGENIC MOUSE;

ADULT; AGED, 80 AND OVER; ANIMALS; CELL SURVIVAL; CELLS, CULTURED; FEMALE; FETUS; HIV-1; HUMANS; INFLAMMASOMES; INFLAMMATION; INFLAMMATION MEDIATORS; MALE; MICE; MICE, TRANSGENIC; MICROGLIA; MIDDLE AGED; NLR FAMILY, PYRIN DOMAIN-CONTAINING 3 PROTEIN; VPR GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

EID: 84990886707     PISSN: 15571890     EISSN: 15571904     Source Type: Journal    
DOI: 10.1007/s11481-016-9708-3     Document Type: Article

References (79)

1. Acharjee S et al. (2010) HIV-1 viral protein R causes peripheral nervous system injury associated with in vivo neuropathic pain. FASEB J 24:4343–4353. doi:10.1096/fj.10-162313
2. Acharjee S, Nayani N, Tsutsui M, Hill MN, Ousman SS, Pittman QJ (2013) Altered cognitive-emotional behavior in early experimental autoimmune encephalitis--cytokine and hormonal correlates. Brain Behav Immun 33:164–172. doi:10.1016/j.bbi.2013.07.003
3. Balasubramanyam A et al. (2007) Effects of transgenic expression of HIV-1 vpr on lipid and energy metabolism in mice. Am J Physiol Endocrinol Metab 292:E40–E48. doi:10.1152/ajpendo.00163.2006
4. Bauernfeind FG et al. (2009) Cutting edge: NF-kappaB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J Immunol 183:787–791. doi:10.4049/jimmunol.0901363
5. Brabers NA, Nottet HS (2006) Role of the pro-inflammatory cytokines TNF-alpha and IL-1beta in HIV-associated dementia. Eur J Clin Investig 36:447–458. doi:10.1111/j.1365-2362.2006.01657.x
6. Brough D, Rothwell NJ (2007) Caspase-1-dependent processing of pro-interleukin-1beta is cytosolic and precedes cell death. J Cell Sci 120:772–781. doi:10.1242/jcs.03377
7. Bryan NB, Dorfleutner A, Rojanasakul Y, Stehlik C (2009) Activation of inflammasomes requires intracellular redistribution of the apoptotic speck-like protein containing a caspase recruitment domain. J Immunol 182:3173–3182. doi:10.4049/jimmunol.0802367
8. Carvour ML, Harms JP, Lynch CF, Mayer RR, Meier JL, Liu D, Torner JC (2015) Differential survival for men and women with HIV/AIDS-related neurologic diagnoses. PLoS One 10:e0123119. doi:10.1371/journal.pone.0123119
9. Chang JR et al. (2011) HIV-1 Tat protein promotes neuronal dysfunction through disruption of microRNAs. J Biol Chem 286:41125–41134. doi:10.1074/jbc.M111.268466
10. Chanput W, Mes JJ, Wichers HJ (2014) THP-1 cell line: an in vitro cell model for immune modulation approach. Int Immunopharmacol 23:37–45. doi:10.1016/j.intimp.2014.08.002
11. Cheng X, Mukhtar M, Acheampong EA, Srinivasan A, Rafi M, Pomerantz RJ, Parveen Z (2007) HIV-1 vpr potently induces programmed cell death in the CNS in vivo. DNA Cell Biol 26:116–131. doi:10.1089/dna.2006.0541
12. Connor RI, Chen BK, Choe S, Landau NR (1995) Vpr is required for efficient replication of human immunodeficiency virus type-1 in mononuclear phagocytes. Virology 206:935–944. doi:10.1006/viro.1995.1016
13. Dagenais M, Skeldon A, Saleh M (2012) The inflammasome: in memory of Dr. Jurg Tschopp. Cell Death Differ 19:5–12. doi:10.1038/cdd.2011.159
14. Doitsh G et al. (2014) Cell death by pyroptosis drives CD4 T-cell depletion in HIV-1 infection. Nature 505:509–514. doi:10.1038/nature12940
15. Eckstein DA, Sherman MP, Penn ML, Chin PS, De Noronha CM, Greene WC, Goldsmith MA (2001) HIV-1 vpr enhances viral burden by facilitating infection of tissue macrophages but not nondividing CD4+ T cells. J Exp Med 194:1407–1419
16. Franchi L, Eigenbrod T, Nunez G (2009) Cutting edge: TNF-alpha mediates sensitization to ATP and silica via the NLRP3 inflammasome in the absence of microbial stimulation. J Immunol 183:792–796. doi:10.4049/jimmunol.0900173
17. Fricke I et al. (2006) Mycobacteria induce IFN-gamma production in human dendritic cells via triggering of TLR2. J Immunol 176:5173–5182
18. Gannon P, Khan MZ, Kolson DL (2011) Current understanding of HIV-associated neurocognitive disorders pathogenesis. Curr Opin Neurol 24:275–283. doi:10.1097/WCO.0b013e32834695fb
19. Garcia-Garcia C, Castillo-Alvarez F, Azcona-Gutierrez JM, Herraiz MJ, Ibarra V, Oteo JA (2015) Spinal cord toxoplasmosis in human immunodeficiency virus infection/acquired immunodeficiency syndrome. Infect Dis (Lond) 47:277–282. doi:10.3109/00365548.2014.993421
20. Guha D, Nagilla P, Redinger C, Srinivasan A, Schatten GP, Ayyavoo V (2012) Neuronal apoptosis by HIV-1 vpr: contribution of proinflammatory molecular networks from infected target cells. J Neuroinflammation 9:138. doi:10.1186/1742-2094-9-1381742-2094-9-138 [pii]
21. Guo H, Gao J, Taxman DJ, Ting JP, Su L (2014) HIV-1 infection induces interleukin-1beta production via TLR8 protein-dependent and NLRP3 inflammasome mechanisms in human monocytes. J Biol Chem 289:21716–21726. doi:10.1074/jbc.M114.566620
22. Harezlak J et al. (2011) Persistence of HIV-associated cognitive impairment, inflammation, and neuronal injury in era of highly active antiretroviral treatment. AIDS 25:625–633. doi:10.1097/QAD.0b013e3283427da7
23. He J, Choe S, Walker R, Di Marzio P, Morgan DO, Landau NR (1995) 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 69:6705–6711
24. Hernandez JC, Latz E, Urcuqui-Inchima S (2014) HIV-1 induces the first signal to activate the NLRP3 inflammasome in monocyte-derived macrophages. Intervirology 57:36–42. doi:10.1159/000353902
25. Hoshino S et al. (2007) Vpr in plasma of HIV type 1-positive patients is correlated with the HIV type 1 RNA titers. AIDS Res Hum Retrovir 23:391–397. doi:10.1089/aid.2006.0124
26. Houzet L, Klase Z, Yeung ML, Wu A, Le SY, Quinones M, Jeang KT (2012) The extent of sequence complementarity correlates with the potency of cellular miRNA-mediated restriction of HIV-1. Nucleic Acids Res 40:11684–11696. doi:10.1093/nar/gks912
27. Huang MB, Weeks O, Zhao LJ, Saltarelli M, Bond VC (2000) Effects of extracellular human immunodeficiency virus type 1 vpr protein in primary rat cortical cell cultures. Journal of Neurovirology 6:202–220
28. Hunter MP et al. (2008) Detection of microRNA expression in human peripheral blood microvesicles. PLoS One 3:e3694. doi:10.1371/journal.pone.0003694
29. Iskander S, Walsh KA, Hammond RR (2004) Human CNS cultures exposed to HIV-1 gp120 reproduce dendritic injuries of HIV-1-associated dementia. J Neuroinflammation 1. doi:10.1186/1742-2094-1-7
30. Jana A, Pahan K (2004) Human immunodeficiency virus type 1 gp120 induces apoptosis in human primary neurons through redox-regulated activation of neutral sphingomyelinase. J Neurosci 24:9531–9540. doi:10.1523/JNEUROSCI.3085-04.2004
31. Jenkins Y, Sanchez PV, Meyer BE, Malim MH (2001) Nuclear export of human immunodeficiency virus type 1 Vpr is not required for virion packaging. J Virol 75:8348–8352
32. Jones GJ et al. (2007) HIV-1 vpr causes neuronal apoptosis and in vivo neurodegeneration. J Neurosci 27:3703–3711. doi:10.1523/JNEUROSCI.5522-06.2007
33. Khan NA, Di Cello F, Stins M, Kim KS (2007) Gp120-mediated cytotoxicity of human brain microvascular endothelial cells is dependent on p38 mitogen-activated protein kinase activation. J Neurovirology 13:242–251. doi:10.1080/13550280701286531
34. Kim W et al. (2015) Neuroinflammation-induced interactions between protease-activated receptor 1 and proprotein convertases in HIV-associated neurocognitive disorder. Mol Cell Biol. doi:10.1128/MCB.00764–15
35. Klegeris A, McGeer PL (2001) Inflammatory cytokine levels are influenced by interactions between THP-1 monocytic, U-373 MG astrocytic, and SH-SY5Y neuronal cell lines of human origin. Neurosci Lett 313:41–44
36. Kogan M, Rappaport J (2011) HIV-1 accessory protein vpr: relevance in the pathogenesis of HIV and potential for therapeutic intervention. Retrovirology 8. doi:10.1186/1742-4690-8-25
37. Lee C, Tomkowicz B, Freedman BD, Collman RG (2005) HIV-1 gp120-induced TNF-{alpha} production by primary human macrophages is mediated by phosphatidylinositol-3 (PI-3) kinase and mitogen-activated protein (MAP) kinase pathways. J Leukoc Biol 78:1016–1023. doi:10.1189/jlb.0105056
38. Lee EO, Kim SE, Park HK, Kang JL, Chong YH (2011) Extracellular HIV-1 tat upregulates TNF-alpha dependent MCP-1/CCL2 production via activation of ERK1/2 pathway in rat hippocampal slice cultures: inhibition by resveratrol, a polyphenolic phytostilbene. Exp Neurol 229:399–408. doi:10.1016/j.expneurol.2011.03.006
39. Levy DN, Refaeli Y, Weiner DB (1995) Extracellular Vpr protein increases cellular permissiveness to human immunodeficiency virus replication and reactivates virus from latency. J Virol 69:1243–1252
40. Levy DN, Refaeli Y, MacGregor RR, Weiner DB (1994) Serum vpr regulates productive infection and latency of human immunodeficiency virus type 1. Proc Natl Acad Sci U S A 91:10873–10877
41. Mahalingam S, Collman RG, Patel M, Monken CE, Srinivasan A (1995) Functional analysis of HIV-1 vpr: identification of determinants essential for subcellular localization. Virology 212:331–339. doi:10.1006/viro.1995.1490
42. Mariathasan S et al. (2006) Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440:228–232. doi:10.1038/nature04515
43. Maroso M, Balosso S, Ravizza T, Iori V, Wright CI, French J, Vezzani A (2011) Interleukin-1beta biosynthesis inhibition reduces acute seizures and drug resistant chronic epileptic activity in mice. Neurotherapeutics 8:304–315. doi:10.1007/s13311-011-0039-z
44. Marozsan AJ et al. (2004) Relationships between infectious titer, capsid protein levels, and reverse transcriptase activities of diverse human immunodeficiency virus type 1 isolates. J Virol 78:11130–11141. doi:10.1128/JVI.78.20.11130-11141.2004
45. Martinon F, Tschopp J (2007) Inflammatory caspases and inflammasomes: master switches of inflammation. Cell Death Differ 14:10–22. doi:10.1038/sj.cdd.4402038
46. Martinon F, Burns K, Tschopp J (2002) The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 10:417–426
47. Mashiba M, Collins DR, Terry VH, Collins KL (2014) Vpr overcomes macrophage-specific restriction of HIV-1 Env expression and virion production. Cell Host Microbe 16:722–735. doi:10.1016/j.chom.2014.10.014
48. McArthur JC, Brew BJ, Nath A (2005) Neurological complications of HIV infection. Lancet Neurol 4:543–555. doi:10.1016/S1474-4422(05)70165-4
49. Molina-Holgado F, Toulmond S, Rothwell NJ (2000) Involvement of interleukin-1 in glial responses to lipopolysaccharide: endogenous versus exogenous interleukin-1 actions. J Neuroimmunol 111:1–9
50. Mukerjee R et al. (2008) Involvement of the p53 and p73 transcription factors in neuroAIDS. Cell Cycle 7:2682–2690
51. Murta V, Farias MI, Pitossi FJ, Ferrari CC (2015) Chronic systemic IL-1beta exacerbates central neuroinflammation independently of the blood-brain barrier integrity. J Neuroimmunol 278:30–43. doi:10.1016/j.jneuroim.2014.11.023
52. Na H et al. (2011) Interactions between human immunodeficiency virus (HIV)-1 vpr expression and innate immunity influence neurovirulence. Retrovirology 8:44. doi:10.1186/1742-4690-8-44
53. Nightingale S, Winston A, Letendre S, Michael BD, McArthur JC, Khoo S, Solomon T (2014) Controversies in HIV-associated neurocognitive disorders. Lancet Neurol 13:1139–1151. doi:10.1016/S1474-4422(14)70137-1
54. Noorbakhsh F et al. (2006) Proteinase-activated receptor 2 modulates neuroinflammation in experimental autoimmune encephalomyelitis and multiple sclerosis. J Exp Med 203:425–435. doi:10.1084/jem.20052148
55. Noorbakhsh F et al. (2010) MicroRNA profiling reveals new aspects of HIV neurodegeneration: caspase-6 regulates astrocyte survival. FASEB J 24:1799–1812. doi:10.1096/fj.09-147819
56. Patel CA, Mukhtar M, Pomerantz RJ (2000) Human immunodeficiency virus type 1 Vpr induces apoptosis in human neuronal cells. J Virol 74:9717–9726
57. Piller SC, Jans P, Gage PW, Jans DA (1998) Extracellular HIV-1 virus protein R causes a large inward current and cell death in cultured hippocampal neurons: implications for AIDS pathology. Proc Natl Acad Sci U S A 95:4595–4600
58. Power C et al. (1998) Neuronal death induced by brain-derived human immunodeficiency virus type 1 envelope genes differs between demented and nondemented AIDS patients. J Virol 72:9045–9053
59. Power C, Hui E, Vivithanaporn P, Acharjee S, Polyak M (2012) Delineating HIV-associated neurocognitive disorders using transgenic models: the neuropathogenic actions of vpr. J NeuroImmune Pharmacol 7:319–331. doi:10.1007/s11481-011-9310-7
60. Ramesh G, MacLean AG, Philipp MT (2013) Cytokines and chemokines at the crossroads of neuroinflammation, neurodegeneration, and neuropathic pain. Mediat Inflamm 2013:480739. doi:10.1155/2013/480739
61. Rao VR, Ruiz AP, Prasad VR (2014) Viral and cellular factors underlying neuropathogenesis in HIV associated neurocognitive disorders (HAND. AIDS Res Ther 11:13. doi:10.1186/1742-6405-11-13)
62. Reinke SN, Broadhurst DL, Sykes BD, Baker GB, Catz I, Warren KG, Power C (2014) Metabolomic profiling in multiple sclerosis: insights into biomarkers and pathogenesis. Mult Scler 20:1396–1400. doi:10.1177/1352458513516528
63. Romani B, Glashoff R, Engelbrecht S (2009) Molecular and phylogenetic analysis of HIV type 1 vpr sequences of South African strains. AIDS Res Hum Retrovir 25:357–362. doi:10.1089/aid.2008.0251
64. Sato K et al. (2013) HIV-1 vpr accelerates viral replication during acute infection by exploitation of proliferating CD4+ T cells in vivo. PLoS Pathog 9:e1003812. doi:10.1371/journal.ppat.1003812
65. Schupbach J (2003) Viral RNA and p24 antigen as markers of HIV disease and antiretroviral treatment success. Int Arch Allergy Immunol 132:196–209. doi:10.1159/000074552
66. Seibenhener ML, Wooten MC (2015) Use of the Open Field Maze to measure locomotor and anxiety-like behavior in mice. J Vis Exp:e52434. doi:10.3791/52434
67. Stack JH, Beaumont K, Larsen PD, Straley KS, Henkel GW, Randle JC, Hoffman HM (2005) IL-converting enzyme/caspase-1 inhibitor VX-765 blocks the hypersensitive response to an inflammatory stimulus in monocytes from familial cold autoinflammatory syndrome patients. J Immunol 175:2630–2634
68. Stewart SA, Poon B, Song JY, Chen IS (2000) Human immunodeficiency virus type 1 vpr induces apoptosis through caspase activation. J Virol 74:3105–3111
69. Strazza M, Pirrone V, Wigdahl B, Nonnemacher MR (2011) Breaking down the barrier: the effects of HIV-1 on the blood-brain barrier. Brain Res 1399:96–115. doi:10.1016/j.brainres.2011.05.015
70. Subbramanian RA, Yao XJ, Dilhuydy H, Rougeau N, Bergeron D, Robitaille Y, Cohen EA (1998) Human immunodeficiency virus type 1 vpr localization: nuclear transport of a viral protein modulated by a putative amphipathic helical structure and its relevance to biological activity. J Mol Biol 278:13–30. doi:10.1006/jmbi.1998.1685
71. Tschopp J, Schroder K (2010) NLRP3 inflammasome activation: the convergence of multiple signalling pathways on ROS production? Nat Rev Immunol 10:210–215. doi:10.1038/nri2725
72. Tungaturthi PK et al. (2003) Role of HIV-1 vpr in AIDS pathogenesis: relevance and implications of intravirion, intracellular and free vpr. Biomed Pharmacother 57:20–24
73. van de Veerdonk FL, Netea MG, Dinarello CA, Joosten LA (2011) Inflammasome activation and IL-1beta and IL-18 processing during infection. Trends Immunol 32:110–116. doi:10.1016/j.it.2011.01.003
74. van der Vos KE, Balaj L, Skog J, Breakefield XO (2011) Brain tumor microvesicles: insights into intercellular communication in the nervous system. Cell Mol Neurobiol 31:949–959. doi:10.1007/s10571-011-9697-y
75. Vigl B, Aebischer D, Nitschke M, Iolyeva M, Rothlin T, Antsiferova O, Halin C (2011) Tissue inflammation modulates gene expression of lymphatic endothelial cells and dendritic cell migration in a stimulus-dependent manner. Blood 118:205–215. doi:10.1182/blood-2010-12-326447
76. Vivithanaporn P et al. (2010) Hepatitis C virus core protein induces neuroimmune activation and potentiates human immunodeficiency virus-1 neurotoxicity. PLoS One 5:e12856. doi:10.1371/journal.pone.0012856e12856
77. Walsh JG et al. (2014) Rapid inflammasome activation in microglia contributes to brain disease in HIV/AIDS. Retrovirology 11:35. doi:10.1186/1742-4690-11-35
78. Wheeler ED, Achim CL, Ayyavoo V (2006) Immunodetection of human immunodeficiency virus type 1 (HIV-1) Vpr in brain tissue of HIV-1 encephalitic patients. Journal of Neurovirology 12:200–210. doi:10.1080/13550280600827377
79. Xiao Y, Chen G, Richard J, Rougeau N, Li H, Seidah NG, Cohen EA (2008) Cell-surface processing of extracellular human immunodeficiency virus type 1 vpr by proprotein convertases. Virology 372:384–397. doi:10.1016/j.virol.2007.10.036