Interactions between human immunodeficiency virus (HIV)-1 Vpr expression and innate immunity influence neurovirulence

Retrovirology

Volumn 8, Issue , 2011, Pages

  Na, Hong ^a   Acharjee, Shaona ^a   Jones, Gareth ^c   Vivithanaporn, Pornpun ^a,d   Noorbakhsh, Farshid ^a   McFarlane, Nicola ^b   Maingat, Ferdinand ^a   Ballanyi, Klaus ^b   Pardo, Carlos A ^e   Cohen, Éric A ^f   Power, Christopher ^a,b,c  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

^c UNIVERSITY OF CALGARY   (Canada)

^d MAHIDOL UNIVERSITY   (Thailand)

^e JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA TUBULIN; VPR PROTEIN; BST2 PROTEIN, HUMAN; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; LEUKOCYTE ANTIGEN; MYXOVIRUS RESISTANCE PROTEINS; VIRUS RNA;

AIDS PATIENT; AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BLOOD; BONE MARROW CELL; BRAIN; CALCIUM TRANSPORT; CONCENTRATION RESPONSE; CONTROLLED STUDY; FETUS; GENE EXPRESSION; GLIA; HIV ASSOCIATED DEMENTIA; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; IMMUNOREACTIVITY; INNATE IMMUNITY; MALE; MOLECULAR CLONING; MOUSE; NERVE CELL LESION; NERVE DEGENERATION; NEUROIMMUNOLOGY; NEUROTOXICITY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; RNA SEQUENCE; SIGNAL TRANSDUCTION; VIRAL TROPISM; VIRUS REPLICATION; VIRUS VIRULENCE; ANIMAL; BIOSYNTHESIS; DNA SEQUENCE; GENE EXPRESSION PROFILING; GENETIC POLYMORPHISM; GENETICS; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; PATHOGENICITY; VIROLOGY;

ANIMALIA; HUMAN IMMUNODEFICIENCY VIRUS 1; MUS;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD; BLOOD; BRAIN; GENE EXPRESSION PROFILING; GPI-LINKED PROTEINS; GTP-BINDING PROTEINS; HIV-1; HUMANS; IMMUNITY, INNATE; INTERFERON-ALPHA; MALE; MICE; MOLECULAR SEQUENCE DATA; NEUROGLIA; POLYMORPHISM, GENETIC; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; VIRAL TROPISM; VPR GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

EID: 79957904923     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-8-44     Document Type: Article

References (95)

1. Chen LF, Hoy J, Lewin SR. Ten years of highly active antiretroviral therapy for HIV infection. Med J Aust 2007, 186:146-151.
2. Barouch DH. Challenges in the development of an HIV-1 vaccine. Nature 2008, 455:613-619. 10.1038/nature07352, 2572109, 18833271.
3. Jaskolski M, Alexandratos JN, Bujacz G, Wlodawer A. Piecing together the structure of retroviral integrase, an important target in AIDS therapy. FEBS J 2009, 276:2926-2946. 10.1111/j.1742-4658.2009.07009.x, 2747025, 19490099.
4. Nikolopoulos G, Bonovas S, Tsantes A, Sitaras NM. HIV/AIDS: recent advances in antiretroviral agents. Mini Rev Med Chem 2009, 9:900-910.
5. Woodman Z, Williamson C. HIV molecular epidemiology: transmission and adaptation to human populations. Curr Opin HIV AIDS 2009, 4:247-252. 10.1097/COH.0b013e32832c0672, 19532060.
6. Letendre SL, McCutchan JA, Childers ME, Woods SP, Lazzaretto D, Heaton RK, Grant I, Ellis RJ. Enhancing antiretroviral therapy for human immunodeficiency virus cognitive disorders. Ann Neurol 2004, 56:416-423. 10.1002/ana.20198, 15349869.
7. Langford D, Marquie-Beck J, de Almeida S, Lazzaretto D, Letendre S, Grant I, McCutchan JA, Masliah E, Ellis RJ. Relationship of antiretroviral treatment to postmortem brain tissue viral load in human immunodeficiency virus-infected patients. J Neurovirol 2006, 12:100-107. 10.1080/13550280600713932, 16798671.
8. Wynn HE, Brundage RC, Fletcher CV. Clinical implications of CNS penetration of antiretroviral drugs. CNS Drugs 2002, 16:595-609. 10.2165/00023210-200216090-00002, 12153332.
9. McArthur JC, Brew BJ, Nath A. Neurological complications of HIV infection. Lancet Neurol 2005, 4:543-555. 10.1016/S1474-4422(05)70165-4, 16109361.
10. Gonzalez-Scarano F, Martin-Garcia J. The neuropathogenesis of AIDS. Nat Rev Immunol 2005, 5:69-81. 10.1038/nri1527, 15630430.
11. Jayadev S, Garden GA. Host and viral factors influencing the pathogenesis of HIV-associated neurocognitive disorders. J Neuroimmune Pharmacol 2009, 4:175-189. 10.1007/s11481-009-9154-6, 2775061, 19373562.
12. Petito CK, Kerza-Kwiatecki AP, Gendelman HE, McCarthy M, Nath A, Podack ER, Shapshak P, Wiley CA. Review: neuronal injury in HIV infection. J Neurovirol 1999, 5:327-341. 10.3109/13550289909029474, 10463855.
13. Doble A. The role of excitotoxicity in neurodegenerative disease: implications for therapy. Pharmacol Ther 1999, 81:163-221. 10.1016/S0163-7258(98)00042-4, 10334661.
14. Nishida K, Markey SP, Kustova Y, Morse HC, Skolnick P, Basile AS, Sei Y. Increased brain levels of platelet-activating factor in a murine acquired immune deficiency syndrome are NMDA receptor-mediated. J Neurochem 1996, 66:433-435.
15. Andersen JL, Le Rouzic E, Planelles V. HIV-1 Vpr: mechanisms of G2 arrest and apoptosis. Exp Mol Pathol 2008, 85:2-10. 10.1016/j.yexmp.2008.03.015, 2610539, 18514189.
16. Moon HS, Yang JS. Role of HIV Vpr as a regulator of apoptosis and an effector on bystander cells. Mol Cells 2006, 21:7-20.
17. Miles MC, Janket ML, Wheeler ED, Chattopadhyay A, Majumder B, Dericco J, Schafer EA, Ayyavoo V. Molecular and functional characterization of a novel splice variant of ANKHD1 that lacks the KH domain and its role in cell survival and apoptosis. FEBS J 2005, 272:4091-4102. 10.1111/j.1742-4658.2005.04821.x, 16098192.
18. Planelles V, Benichou S. Vpr and its interactions with cellular proteins. Curr Top Microbiol Immunol 339:177-200.
19. Kilareski EM, Shah S, Nonnemacher MR, Wigdahl B. Regulation of HIV-1 transcription in cells of the monocyte-macrophage lineage. Retrovirology 2009, 6:118. 10.1186/1742-4690-6-118, 2805609, 20030845.
20. 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, 27:3703-3711. 10.1523/JNEUROSCI.5522-06.2007, 17409234.
21. 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, 82:2528-2542. 10.1128/JVI.02094-07, 2258941, 18094160.
22. Patel CA, Mukhtar M, Pomerantz RJ. Human immunodeficiency virus type 1 Vpr induces apoptosis in human neuronal cells. J Virol 2000, 74:9717-9726. 10.1128/JVI.74.20.9717-9726.2000, 112404, 11000244.
23. Sanchez MS, Grant RM, Porco TC, Getz WM. HIV drug-resistant strains as epidemiologic sentinels. Emerg Infect Dis 2006, 12:191-197.
24. Smit TK, Brew BJ, Tourtellotte W, Morgello S, Gelman BB, Saksena NK. Independent evolution of human immunodeficiency virus (HIV) drug resistance mutations in diverse areas of the brain in HIV-infected patients, with and without dementia, on antiretroviral treatment. J Virol 2004, 78:10133-10148. 10.1128/JVI.78.18.10133-10148.2004, 515019, 15331746.
25. Tcherepanova I, Starr A, Lackford B, Adams MD, Routy JP, Boulassel MR, Calderhead D, Healey D, Nicolette C. The immunosuppressive properties of the HIV Vpr protein are linked to a single highly conserved residue, R90. PLoS One 2009, 4:e5853. 10.1371/journal.pone.0005853, 2689350, 19516896.
26. Nakaya T, Fujinaga K, Kishi M, Oka S, Kurata T, Jones IM, Ikuta K. Nonsense mutations in the vpr gene of HIV-1 during in vitro virus passage and in HIV-1 carrier-derived peripheral blood mononuclear cells. FEBS Lett 1994, 354:17-22. 10.1016/0014-5793(94)01074-9, 7957894.
27. Lum JJ, Cohen OJ, Nie Z, Weaver JG, Gomez TS, Yao XJ, Lynch D, Pilon AA, Hawley N, Kim JE, et al. Vpr R77Q is associated with long-term nonprogressive HIV infection and impaired induction of apoptosis. J Clin Invest 2003, 111:1547-1554. 155040, 12750404.
28. Rajan D, Wildum S, Rucker E, Schindler M, Kirchhoff F. Effect of R77Q, R77A and R80A changes in Vpr on HIV-1 replication and CD4 T cell depletion in human lymphoid tissue ex vivo. AIDS 2006, 20:831-836. 10.1097/01.aids.0000218546.31716.7f, 16549966.
29. Mologni D, Citterio P, Menzaghi B, Zanone Poma B, Riva C, Broggini V, Sinicco A, Milazzo L, Adorni F, Rusconi S, et al. Vpr and HIV-1 disease progression: R77Q mutation is associated with long-term control of HIV-1 infection in different groups of patients. AIDS 2006, 20:567-574. 10.1097/01.aids.0000210611.60459.0e, 16470121.
30. Pomerantz RJ. Effects of HIV-1 Vpr on neuroinvasion and neuropathogenesis. DNA Cell Biol 2004, 23:227-238. 10.1089/104454904773819815, 15142380.
31. Mattson MP, Haughey NJ, Nath A. Cell death in HIV dementia. Cell Death Differ 2005, 12(Suppl 1):893-904.
32. van Marle G, Power C. Human immunodeficiency virus type 1 genetic diversity in the nervous system: evolutionary epiphenomenon or disease determinant?. J Neurovirol 2005, 11:107-128. 10.1080/13550280590922838, 16036790.
33. Wheeler ED, Achim CL, Ayyavoo V. Immunodetection of human immunodeficiency virus type 1 (HIV-1) Vpr in brain tissue of HIV-1 encephalitic patients. J Neurovirol 2006, 12:200-210. 10.1080/13550280600827377, 16877301.
34. 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. J Leukoc Biol 1997, 62:93-99.
35. Yadav A, Collman RG. CNS Inflammation and Macrophage/Microglial Biology Associated with HIV-1 Infection. J Neuroimmune Pharmacol 2009,
36. Chui C, Cheung PK, Brumme CJ, Mo T, Brumme ZL, Montaner JS, Badley AD, Harrigan PR. HIV VprR77Q mutation does not influence clinical response of individuals initiating highly active antiretroviral therapy. AIDS Res Hum Retroviruses 2006, 22:615-618. 10.1089/aid.2006.22.615, 2423217, 16831085.
37. Irie T, Nagata N, Yoshida T, Sakaguchi T. Paramyxovirus Sendai virus C proteins are essential for maintenance of negative-sense RNA genome in virus particles. Virology 2008, 374:495-505. 10.1016/j.virol.2008.01.004, 18252261.
38. Majumder B, Janket ML, Schafer EA, Schaubert K, Huang XL, Kan-Mitchell J, Rinaldo CR, Ayyavoo V. Human immunodeficiency virus type 1 Vpr impairs dendritic cell maturation and T-cell activation: implications for viral immune escape. J Virol 2005, 79:7990-8003. 10.1128/JVI.79.13.7990-8003.2005, 1143734, 15956545.
39. Muthumani K, Choo AY, Hwang DS, Dayes NS, Chattergoon M, Mayilvahanan S, Thieu KP, Buckley PT, Emmanuel J, Premkumar A, Weiner DB. HIV-1 Viral protein-r (Vpr) protects against lethal superantigen challenge while maintaining homeostatic T cell levels in vivo. Mol Ther 2005, 12:910-921. 10.1016/j.ymthe.2005.05.009, 16006193.
40. Muthumani K, Hwang DS, Choo AY, Mayilvahanan S, Dayes NS, Thieu KP, Weiner DB. HIV-1 Vpr inhibits the maturation and activation of macrophages and dendritic cells in vitro. Int Immunol 2005, 17:103-116.
41. Kamata M, Wu RP, An DS, Saxe JP, Damoiseaux R, Phelps ME, Huang J, Chen IS. Cell-based chemical genetic screen identifies damnacanthal as an inhibitor of HIV-1 Vpr induced cell death. Biochem Biophys Res Commun 2006, 348:1101-1106. 10.1016/j.bbrc.2006.07.158, 1761125, 16904642.
42. Wang JJ, Lu Y, Ratner L. Particle assembly and Vpr expression in human immunodeficiency virus type 1-infected cells demonstrated by immunoelectron microscopy. J Gen Virol 1994, 75(Pt 10):2607-2614.
43. Vodicka MA, Koepp DM, Silver PA, Emerman M. HIV-1 Vpr interacts with the nuclear transport pathway to promote macrophage infection. Genes Dev 1998, 12:175-185. 10.1101/gad.12.2.175, 316441, 9436978.
44. Sherman MP, De Noronha CM, Williams SA, Greene WC. Insights into the biology of HIV-1 viral protein R. DNA Cell Biol 2002, 21:679-688. 10.1089/104454902760330228, 12396611.
45. Mahalingam S, Ayyavoo V, Patel M, Kieber-Emmons T, Weiner DB. Nuclear import, virion incorporation, and cell cycle arrest/differentiation are mediated by distinct functional domains of human immunodeficiency virus type 1 Vpr. J Virol 1997, 71:6339-6347. 191907, 9261351.
46. Levy DN, Refaeli Y, MacGregor RR, Weiner DB. Serum Vpr regulates productive infection and latency of human immunodeficiency virus type 1. Proc Natl Acad Sci USA 1994, 91:10873-10877. 10.1073/pnas.91.23.10873, 45128, 7971975.
47. Sabbah EN, Roques BP. Critical implication of the (70-96) domain of human immunodeficiency virus type 1 Vpr protein in apoptosis of primary rat cortical and striatal neurons. J Neurovirol 2005, 11:489-502. 10.1080/13550280500384941, 16338743.
48. Amini S, Khalili K, Sawaya BE. Effect of HIV-1 Vpr on cell cycle regulators. DNA Cell Biol 2004, 23:249-260. 10.1089/104454904773819833, 15142382.
49. Patel CA, Mukhtar M, Harley S, Kulkosky J, Pomerantz RJ. Lentiviral expression of HIV-1 Vpr induces apoptosis in human neurons. J Neurovirol 2002, 8:86-99. 10.1080/13550280290049552, 11935461.
50. Conti L, Rainaldi G, Matarrese P, Varano B, Rivabene R, Columba S, Sato A, Belardelli F, Malorni W, Gessani S. The HIV-1 vpr protein acts as a negative regulator of apoptosis in a human lymphoblastoid T cell line: possible implications for the pathogenesis of AIDS. J Exp Med 1998, 187:403-413. 10.1084/jem.187.3.403, 2212119, 9449720.
51. Snyder A, Alsauskas Z, Gong P, Rosenstiel PE, Klotman ME, Klotman PE, Ross MJ. FAT10: a novel mediator of Vpr-induced apoptosis in human immunodeficiency virus-associated nephropathy. J Virol 2009, 83:11983-11988. 10.1128/JVI.00034-09, 2772664, 19726511.
52. Andersen JL, DeHart JL, Zimmerman ES, Ardon O, Kim B, Jacquot G, Benichou S, Planelles V. HIV-1 Vpr-induced apoptosis is cell cycle dependent and requires Bax but not ANT. PLoS Pathog 2006, 2:e127. 10.1371/journal.ppat.0020127, 1665652, 17140287.
53. Roshal M, Zhu Y, Planelles V. Apoptosis in AIDS. Apoptosis 2001, 6:103-116. 10.1023/A:1009636530839, 11321033.
54. Xiao Y, Chen G, Richard J, Rougeau N, Li H, Seidah NG, Cohen EA. Cell-surface processing of extracellular human immunodeficiency virus type 1 Vpr by proprotein convertases. Virology 2008, 372:384-397. 10.1016/j.virol.2007.10.036, 18061232.
55. Ferri KF, Jacotot E, Blanco J, Este JA, Kroemer G. Mitochondrial control of cell death induced by HIV-1-encoded proteins. Ann N Y Acad Sci 2000, 926:149-164.
56. Piller SC, Ewart GD, Jans DA, Gage PW, Cox GB. The amino-terminal region of Vpr from human immunodeficiency virus type 1 forms ion channels and kills neurons. J Virol 1999, 73:4230-4238. 104202, 10196319.
57. van de Bovenkamp M, Nottet HS, Pereira CF. Interactions of human immunodeficiency virus-1 proteins with neurons: possible role in the development of human immunodeficiency virus-1-associated dementia. Eur J Clin Invest 2002, 32:619-627. 10.1046/j.1365-2362.2002.01029.x, 12190962.
58. Persidsky Y, Poluektova L. Immune privilege and HIV-1 persistence in the CNS. Immunol Rev 2006, 213:180-194. 10.1111/j.1600-065X.2006.00440.x, 16972904.
59. Clerici M, Stocks NI, Zajac RA, Boswell RN, Bernstein DC, Mann DL, Shearer GM, Berzofsky JA. Interleukin-2 production used to detect antigenic peptide recognition by T-helper lymphocytes from asymptomatic HIV-seropositive individuals. Nature 1989, 339:383-385. 10.1038/339383a0, 2524668.
60. DeVico AL, Gallo RC. Control of HIV-1 infection by soluble factors of the immune response. Nat Rev Microbiol 2004, 2:401-413. 10.1038/nrmicro878, 15100693.
61. Haller O, Staeheli P, Kochs G. Interferon-induced Mx proteins in antiviral host defense. Biochimie 2007, 89:812-818. 10.1016/j.biochi.2007.04.015, 17570575.
62. Sadler AJ, Williams BR. Interferon-inducible antiviral effectors. Nat Rev Immunol 2008, 8:559-568. 10.1038/nri2314, 2522268, 18575461.
63. Van Damme N, Goff D, Katsura C, Jorgenson RL, Mitchell R, Johnson MC, Stephens EB, Guatelli J. The interferon-induced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell Host Microbe 2008, 3:245-252. 10.1016/j.chom.2008.03.001, 2474773, 18342597.
64. Haller O, Staeheli P, Kochs G. Protective role of interferon-induced Mx GTPases against influenza viruses. Rev Sci Tech 2009, 28:219-231.
65. Daher A, Laraki G, Singh M, Melendez-Pena CE, Bannwarth S, Peters AH, Meurs EF, Braun RE, Patel RC, Gatignol A. TRBP control of PACT-induced phosphorylation of protein kinase R is reversed by stress. Mol Cell Biol 2009, 29:254-265. 10.1128/MCB.01030-08, 2612476, 18936160.
66. Tokarev A, Skasko M, Fitzpatrick K, Guatelli J. Antiviral activity of the interferon-induced cellular protein BST-2/tetherin. AIDS Res Hum Retroviruses 2009, 25:1197-1210. 2858902, 19929170.
67. Rho MB, Wesselingh S, Glass JD, McArthur JC, Choi S, Griffin J, Tyor WR. A potential role for interferon-alpha in the pathogenesis of HIV-associated dementia. Brain Behav Immun 1995, 9:366-377. 10.1006/brbi.1995.1034, 8903853.
68. Sas AR, Bimonte-Nelson H, Smothers CT, Woodward J, Tyor WR. Interferon-alpha causes neuronal dysfunction in encephalitis. J Neurosci 2009, 29:3948-3955. 10.1523/JNEUROSCI.5595-08.2009, 19321791.
69. Raber J, Sorg O, Horn TF, Yu N, Koob GF, Campbell IL, Bloom FE. Inflammatory cytokines: putative regulators of neuronal and neuro-endocrine function. Brain Res Brain Res Rev 1998, 26:320-326.
70. Ritola K, Robertson K, Fiscus SA, Hall C, Swanstrom R. Increased human immunodeficiency virus type 1 (HIV-1) env compartmentalization in the presence of HIV-1-associated dementia. J Virol 2005, 79:10830-10834. 10.1128/JVI.79.16.10830-10834.2005, 1182623, 16051875.
71. Power C, McArthur JC, Nath A, Wehrly K, Mayne M, Nishio J, Langelier T, Johnson RT, Chesebro B. Neuronal death induced by brain-derived human immunodeficiency virus type 1 envelope genes differs between demented and nondemented AIDS patients. J Virol 1998, 72:9045-9053. 110321, 9765449.
72. Power C, McArthur JC, Johnson RT, Griffin DE, Glass JD, Perryman S, Chesebro B. Demented and nondemented patients with AIDS differ in brain-derived human immunodeficiency virus type 1 envelope sequences. J Virol 1994, 68:4643-4649. 236392, 8207838.
73. Dunfee RL, Thomas ER, Wang J, Kunstman K, Wolinsky SM, Gabuzda D. Loss of the N-linked glycosylation site at position 386 in the HIV envelope V4 region enhances macrophage tropism and is associated with dementia. Virology 2007, 367:222-234. 10.1016/j.virol.2007.05.029, 2201988, 17599380.
74. Bratanich AC, Liu C, McArthur JC, Fudyk T, Glass JD, Mittoo S, Klassen GA, Power C. Brain-derived HIV-1 tat sequences from AIDS patients with dementia show increased molecular heterogeneity. J Neurovirol 1998, 4:387-393. 10.3109/13550289809114537, 9718130.
75. Mayne M, Bratanich AC, Chen P, Rana F, Nath A, Power C. HIV-1 tat molecular diversity and induction of TNF-alpha: implications for HIV-induced neurological disease. Neuroimmunomodulation 1998, 5:184-192. 10.1159/000026336, 9730685.
76. Van Marle G, Rourke SB, Zhang K, Silva C, Ethier J, Gill MJ, Power C. HIV dementia patients exhibit reduced viral neutralization and increased envelope sequence diversity in blood and brain. AIDS 2002, 16:1905-1914. 10.1097/00002030-200209270-00007, 12351950.
77. Churchill MJ, Wesselingh SL, Cowley D, Pardo CA, McArthur JC, Brew BJ, Gorry PR. Extensive astrocyte infection is prominent in human immunodeficiency virus-associated dementia. Ann Neurol 2009, 66:253-258. 10.1002/ana.21697, 19743454.
78. Tucker PC, Lee SH, Bui N, Martinie D, Griffin DE. Amino acid changes in the Sindbis virus E2 glycoprotein that increase neurovirulence improve entry into neuroblastoma cells. J Virol 1997, 71:6106-6112. 191871, 9223505.
79. Zink MC, Spelman JP, Robinson RB, Clements JE. SIV infection of macaques--modeling the progression to AIDS dementia. J Neurovirol 1998, 4:249-259. 10.3109/13550289809114526, 9639068.
80. Zhou Y, Ratner L. Phosphorylation of human immunodeficiency virus type 1 Vpr regulates cell cycle arrest. J Virol 2000, 74:6520-6527. 10.1128/JVI.74.14.6520-6527.2000, 112161, 10864665.
81. Agostini I, Popov S, Hao T, Li JH, Dubrovsky L, Chaika O, Chaika N, Lewis R, Bukrinsky M. Phosphorylation of Vpr regulates HIV type 1 nuclear import and macrophage infection. AIDS Res Hum Retroviruses 2002, 18:283-288. 10.1089/088922202753472856, 11860675.
82. McArthur JC, Hoover DR, Bacellar H, Miller EN, Cohen BA, Becker JT, Graham NM, McArthur JH, Selnes OA, Jacobson LP, et al. Dementia in AIDS patients: incidence and risk factors. Multicenter AIDS Cohort Study. Neurology 1993, 43:2245-2252.
83. Vivithanaporn P, Heo G, Gamble J, Krentz H, Hoke A, Gill J, Power C. Neurologic disease burden in treated HIV/AIDS predicts survival: a population-based study. Neurology 2010,
84. Noorbakhsh F, Ramachandran R, Barsby B, 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. The FASEB Journal 2010,
85. van Marle G, Henry S, Todoruk T, Sullivan A, Silva C, Rourke SB, Holden J, McArthur JC, Gill MJ, Power C. Human immunodeficiency virus type 1 Nef protein mediates neural cell death: a neurotoxic role for IP-10. Virology 2004, 329:302-318.
86. Zhu Y, Vergote D, Pardo C, Noorbakhsh F, McArthur JC, Hollenberg MD, Overall CM, Power C. CXCR3 activation by lentivirus infection suppresses neuronal autophagy: neuroprotective effects of antiretroviral therapy. FASEB J 2009, 23:2928-2941. 10.1096/fj.08-128819, 2796902, 19380511.
87. Yao XJ, Mouland AJ, Subbramanian RA, Forget J, Rougeau N, Bergeron D, Cohen EA. Vpr stimulates viral expression and induces cell killing in human immunodeficiency virus type 1-infected dividing Jurkat T cells. J Virol 1998, 72:4686-4693. 109992, 9573232.
88. Subbramanian RA, Yao XJ, Dilhuydy H, Rougeau N, Bergeron D, Robitaille Y, Cohen EA. 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 1998, 278:13-30. 10.1006/jmbi.1998.1685, 9571031.
89. Johnston JB, Jiang Y, van Marle G, Mayne MB, Ni W, Holden J, McArthur JC, Power C. Lentivirus infection in the brain induces matrix metalloproteinase expression: role of envelope diversity. J Virol 2000, 74:7211-7220. 10.1128/JVI.74.16.7211-7220.2000, 112242, 10906175.
90. Power C, Henry S, Del Bigio MR, Larsen PH, Corbett D, Imai Y, Yong VW, Peeling J. Intracerebral hemorrhage induces macrophage activation and matrix metalloproteinases. Ann Neurol 2003, 53:731-742. 10.1002/ana.10553, 12783419.
91. Levy DN, Refaeli Y, MacGregor RR, DB W. Serum Vpr regulates productive infection and latency of human immunodeficiency virus type 1. Proc Natl Acad Sci USA 1994, 91:10873-10877. 10.1073/pnas.91.23.10873, 45128, 7971975.
92. Ruangkittisakul A, Schwarzacher Stephan W, Lucia S, Poon Betty Y, Yonglie M, Funk Gregory D, Klaus B. High Sensitivity to Neuromodulator-Activated Signaling Pathways at Physiological [K+] of Confocally Imaged Respiratory Center Neurons in On-Line-Calibrated Newborn Rat Brainstem Slices. J Neurosci 2006, 26:11870-11880. 10.1523/JNEUROSCI.3357-06.2006, 17108160.
93. Silva C, Zhang K, Tsutsui S, Holden JK, Gill MJ, Power C. Growth hormone prevents human immunodeficiency virus-induced neuronal p53 expression. Ann Neurol 2003, 54:605-614. 10.1002/ana.10729, 14595650.
94. Ungerstedt U, Arbuthnott GW. Quantitative recording of rotational behavior in rats after 6-hydroxy-dopamine lesions of the nigrostriatal dopamine system. Brain Res 1970, 24:485-493. 10.1016/0006-8993(70)90187-3, 5494536.
95. Tsutsui S, Schnermann J, Noorbakhsh F, Henry S, Yong VW, Winston BW, Warren K, Power C. A1 adenosine receptor upregulation and activation attenuates neuroinflammation and demyelination in a model of multiple sclerosis. J Neurosci 2004, 24:1521-1529. 10.1523/JNEUROSCI.4271-03.2004, 14960625.