Transgenic mice expressing HIV-1 envelope protein gp120 in the brain as an animal model in neuroAIDS research

Journal of NeuroVirology

Volumn 24, Issue 2, 2018, Pages 156-167

  Thaney, Victoria E ^a   Sanchez, Ana B ^a   Fields, Jerel A ^b   Minassian, Arpi ^b   Young, Jared W ^b   Maung, Ricky ^a   Kaul, Marcus ^a,b,c  

^a BURNHAM INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

gp120; HAND; HIV 1; NeuroAIDS; Neuroprotection; Transgenic animal model

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; GLYCOPROTEIN GP 120; FUSION PROTEIN; GLIAL FIBRILLARY ASTROCYTIC PROTEIN, MOUSE; GP120 PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; AIDS PATIENT; ANIMAL BEHAVIOR; ASTROCYTOSIS; BEHAVIOR CHANGE; BRAIN; BRAIN INJURY; CLINICAL FEATURE; DENDRITIC CELL; DRUG ABUSE; HIV ASSOCIATED DEMENTIA; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; INNATE IMMUNITY; LEARNING DISORDER; MICROGLIA; MOUSE MODEL; NERVOUS SYSTEM DEVELOPMENT; NEUROPATHOLOGY; NEUROTOXICITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; ANIMAL; ASTROCYTE; CHEMISTRY; COGNITIVE DEFECT; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; MOUSE; PATHOLOGY; PATHOPHYSIOLOGY; SYNAPSE;

AIDS DEMENTIA COMPLEX; ANIMALS; ASTROCYTES; BRAIN; COGNITIVE DYSFUNCTION; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; HIV ENVELOPE PROTEIN GP120; HIV-1; IMMUNITY, INNATE; MICE; MICE, TRANSGENIC; PROMOTER REGIONS, GENETIC; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 85032368618     PISSN: 13550284     EISSN: 15382443     Source Type: Journal    
DOI: 10.1007/s13365-017-0584-2     Document Type: Review

References (128)

1. Adle-Biassette H, Levy Y, Colombel M, Poron F, Natchev S, Keohane C, Gray F (1995) Neuronal apoptosis in HIV infection in adults. Neuropathol Appl Neurobiol 21:218–227
2. Ambrose Z, Kewalramani VN, Bieniasz PD, Hatziioannou T (2007) HIV/ AIDS: in search of an animal model. Trends Biotechnol 25:333–337
3. Antinori A, Arendt G, Becker JT, Brew BJ, Byrd DA, Cherner M, Clifford DB, Cinque P, Epstein LG, Goodkin K, Gisslen M, Grant I, Heaton RK, Joseph J, Marder K, Marra CM, McArthur JC, Nunn M, Price RW, Pulliam L, Robertson KR, Sacktor N, Valcour V, Wojna VE (2007) Updated research nosology for HIV-associated neurocognitive disorders. Neurology 69:1789–1799
4. 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
5. Avdoshina V, Fields JA, Castellano P, Dedoni S, Palchik G, Trejo M, Adame A, Rockenstein E, Eugenin E, Masliah E, Mocchetti I (2016) The HIV protein gp120 alters mitochondrial dynamics in neurons. Neurotox Res 29:583–593
6. Avraham HK, Jiang S, Fu Y, Rockenstein E, Makriyannis A, Zvonok A, Masliah E, Avraham S (2014) The cannabinoid CB(2) receptor agonist AM1241 enhances neurogenesis in GFAP/Gp120 transgenic mice displaying deficits in neurogenesis. Br J Pharmacol 171:468– 479
7. Avraham HK, Jiang S, Fu Y, Rockenstein E, Makriyannis A, Wood J, Wang L, Masliah E, Avraham S (2015) Impaired neurogenesis by HIV-1-Gp120 is rescued by genetic deletion of fatty acid amide hydrolase enzyme. Br J Pharmacol 172:4603–4614
8. Bachis A, Aden SA, Nosheny RL, Andrews PM, Mocchetti I (2006) Axonal transport of human immunodeficiency virus type 1 envelope protein glycoprotein 120 is found in association with neuronal apoptosis. J Neurosci 26:6771–6780
9. Bachis A, Forcelli P, Masliah E, Campbell L, Mocchetti I (2016) Expression of gp120 in mice evokes anxiety behavior: co-occurrence with increased dendritic spines and brain-derived neurotrophic factor in the amygdala. Brain Behav Immun 54:170–177
10. Bae M, Patel N, Xu H, Lee M, Tominaga-Yamanaka K, Nath A, Geiger J, Gorospe M, Mattson MP, Haughey NJ (2014) Activation of TRPML1 clears intraneuronal Abeta in preclinical models of HIV infection. J Neurosci 34:11485–11503
11. Bandaru VV, Patel N, Ewaleifoh O, Haughey NJ (2011) A failure to normalize biochemical and metabolic insults during morphine withdrawal disrupts synaptic repair in mice transgenic for HIV-gp120. J NeuroImmune Pharmacol 6:640–649
12. Banerjee S, Liao L, Russo R, Nakamura T, McKercher SR, Okamoto S, Haun F, Nikzad R, Zaidi R, Holland E, Eroshkin A, Yates JR III, Lipton SA (2012) Isobaric tagging-based quantification by mass spectrometry of differentially regulated proteins in synaptosomes of HIV/gp120 transgenic mice: implications for HIV-associated neurodegeneration. Exp Neurol 236:298–306
13. Barber SA, Herbst DS, Bullock BT, Gama L, Clements JE (2004) Innate immune responses and control of acute simian immunodeficiency virus replication in the central nervous system. J Neuro-Oncol 10(Suppl 1):15–20
14. Barre-Sinoussi F, Chermann JC, Rey F, Nugeyre MT, Chamaret S, Gruest J, Dauguet C, Axler-Blin C, Vezinet-Brun F, Rouzioux C, Rozenbaum W, Montagnier L (1983) Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS). Science 220:868–871
15. Berrada F, Ma D, Michaud J, Doucet G, Giroux L, Kessous-Elbaz A (1995) Neuronal expression of human immunodeficiency virus type 1 env proteins in transgenic mice: distribution in the central nervous system and pathological alterations. J Virol 69:6770–6778
16. Brew BJ, Crowe SM, Landay A, Cysique LA, Guillemin G (2009) Neurodegeneration and ageing in the HAART era. J NeuroImmune Pharmacol 4:163–174
17. Brew BJ, Robertson K, Wright EJ, Churchill M, Crowe SM, Cysique LA, Deeks S, Garcia JV, Gelman B, Gray LR, Johnson T, Joseph J, Margolis DM, Mankowski JL, Spencer B (2015) HIV eradication symposium: will the brain be left behind? J Neuro-Oncol 21:322– 334
18. Bruce-Keller AJ, Turchan-Cholewo J, Smart EJ, Geurin T, Chauhan A, Reid R, Xu R, Nath A, Knapp PE, Hauser KF (2008) Morphine causes rapid increases in glial activation and neuronal injury in the striatum of inducible HIV-1 Tat transgenic mice. Glia 56:1414–1427
19. Carey CL, Woods SP, Rippeth JD, Gonzalez R, Heaton RK, Grant I (2006) Additive deleterious effects of methamphetamine dependence and immunosuppression on neuropsychological functioning in HIV infection. AIDS Behav 10:185–190
20. Chang SL, Connaghan KP, Wei Y, Li MD (2014) NeuroHIV and use of addictive substances. Int Rev Neurobiol 118:403–440
21. Chatterjee N, Callen S, Seigel GM, Buch SJ (2011) HIV-1 Tat-mediated neurotoxicity in retinal cells. J NeuroImmune Pharmacol 6:399–408
22. Churchill M, Nath A (2013). Where does HIV hide? A focus on the central nervous system. Curr Opin HIV AIDS. 8:165–169
23. Clements JE, Anderson MG, Zink MC, Joag SV, Narayan O (1994) The SIV model of AIDS encephalopathy. Role of neurotropic viruses in diseases. Res Publ Assoc Res Nerv Ment Dis 72:147–157
24. Clements JE, Mankowski JL, Gama L, Zink MC (2008) The accelerated simian immunodeficiency virus macaque model of human immunodeficiency virus-associated neurological disease: from mechanism to treatment. J Neuro-Oncol 14:309–317
25. Crews L, Ruf R, Patrick C, Dumaop W, Trejo-Morales M, Achim CL, Rockenstein E, Masliah E (2011) Phosphorylation of collapsin response mediator protein-2 disrupts neuronal maturation in a model of adult neurogenesis: implications for neurodegenerative disorders. Mol Neurodegener 6:67
26. D'hooge R, Franck F, Mucke L, De Deyn PP (1999) Age-related behavioural deficits in transgenic mice expressing the HIV-1 coat protein gp120. Eur J Neurosci 11:4398–4402
27. Dash PK, Gorantla S, Gendelman HE, Knibbe J, Casale GP, Makarov E, Epstein AA, Gelbard HA, Boska MD, Poluektova LY (2011) Loss of neuronal integrity during progressive HIV-1 infection of humanized mice. J Neurosci 31:3148–3157
28. Doyle T, Goujon C, Malim MH (2015) HIV-1 and interferons: who’s interfering with whom? Nat Rev Microbiol 13:403–413
29. Ferretti F, Gisslen M, Cinque P, Price RW (2015) Cerebrospinal fluid HIV escape from antiretroviral therapy. Curr HIV/AIDS Rep 12:280–288
30. Fields J, Dumaop W, Langford TD, Rockenstein E, Masliah E (2014) Role of neurotrophic factor alterations in the neurodegenerative process in HIV associated neurocognitive disorders. J NeuroImmune Pharmacol 9:102–116
31. Fields J, Dumaop W, Rockenstein E, Mante M, Spencer B, Grant I, Ellis R, Letendre S, Patrick C, Adame A, Masliah E (2013) Age-dependent molecular alterations in the autophagy pathway in HIVE patients and in a gp120 tg mouse model: reversal with beclin-1 gene transfer. J Neuro-Oncol 19:89–101
32. Fields JA, Overk C, Adame A, Florio J, Mante M, Pineda A, Desplats P, Rockenstein E, Achim C, Masliah E (2016a) Neuroprotective effects of the immunomodulatory drug FK506 in a model of HIV1-gp120 neurotoxicity. J Neuroinflammation 13:120
33. Fields JA, Serger E, Campos S, Divakaruni AS, Kim C, Smith K, Trejo M, Adame A, Spencer B, Rockenstein E, Murphy AN, Ellis RJ, Letendre S, Grant I, Masliah E (2016b) HIV alters neuronal mitochondrial fission/fusion in the brain during HIV-associated neurocognitive disorders. Neurobiol Dis 86:154–169
34. Fitting S, Xu R, Bull C, Buch SK, El-Hage N, Nath A, Knapp PE, Hauser KF (2010) Interactive comorbidity between opioid drug abuse and HIV-1 Tat: chronic exposure augments spine loss and sublethal dendritic pathology in striatal neurons. Am J Pathol 177:1397–1410
35. Garden GA, Budd SL, Tsai E, Hanson L, Kaul M, D'Emilia DM, Friedlander RM, Yuan J, Masliah E, Lipton SA (2002) Caspase cascades in human immunodeficiency virus-associated neurodegeneration. J Neurosci 22:4015–4024
36. Gardner MB, Luciw PA (1989) Animal models of AIDS. FASEB J 3: 2593–2606
37. Giulian D, Vaca K, Noonan CA (1990) Secretion of neurotoxins by mononuclear phagocytes infected with HIV-1. Science 250:1593– 1596
38. Gonzalez-Scarano F, Martin-Garcia J (2005) The neuropathogenesis of AIDS. Nat Rev Immunol 5:69–81
39. Gray LR, Roche M, Flynn JK, Wesselingh SL, Gorry PR, Churchill MJ (2014) Is the central nervous system a reservoir of HIV-1? Curr Opin HIV AIDS 9:552–558
40. Green DA, Masliah E, Vinters HV, Beizai P, Moore DJ, Achim CL (2005) Brain deposition of beta-amyloid is a common pathologic feature in HIV positive patients. AIDS 19:407–411
41. Hahn BH, Shaw GM, Arya SK, Popovic M, Gallo RC, Wong-Staal F (1984) Molecular cloning and characterization of the HTLV-III virus associated with AIDS. Nature 312:166–169
42. Hanna Z, Kay DG, Cool M, Jothy S, Rebai N, Jolicoeur P (1998a) Transgenic mice expressing human immunodeficiency virus type 1 in immune cells develop a severe AIDS-like disease. J Virol 72:121– 132
43. Hanna Z, Kay DG, Rebai N, Guimond A, Jothy S, Jolicoeur P (1998b) Nef harbors a major determinant of pathogenicity for an AIDS-like disease induced by HIV-1 in transgenic mice. Cell 95:163–175
44. Hauser KF, Hahn YK, Adjan VV, Zou S, Buch SK, Nath A, Bruce-Keller AJ, Knapp PE (2009) HIV-1 Tat and morphine have interactive effects on oligodendrocyte survival and morphology. Glia 57:194– 206
45. Henry BL, Geyer MA, Buell M, Perry W, Young JW, Minassian A, Translational Methamphetamine ARCG (2013) Behavioral effects of chronic methamphetamine treatment in HIV-1 gp120 transgenic mice. Behav Brain Res 236:210–220
46. Henry BL, Geyer MA, Buell MR, Perry W, Young JW, Minassian A, Translational Methamphetamine ARCG (2014) Prepulse inhibition in HIV-1 gp120 transgenic mice after withdrawal from chronic methamphetamine. Behav Pharmacol 25:12–22
47. Hoefer MM, Sanchez AB, Maung R, de Rozieres CM, Catalan IC, Dowling CC, Thaney VE, Pina-Crespo J, Zhang D, Roberts AJ, Kaul M (2015) Combination of methamphetamine and HIV-1 gp120 causes distinct long-term alterations of behavior, gene expression, and injury in the central nervous system. Exp Neurol 263:221– 234
48. Iwakura Y, Shioda T, Tosu M, Yoshida E, Hayashi M, Nagata T, Shibuta H (1992) The induction of cataracts by HIV-1 in transgenic mice. AIDS 6:1069–1075
49. Jacobson S, Henriksen SJ, Prospero-Garcia O, Phillips TR, Elder JH, Young WG, Bloom FE, Fox HS (1997) Cortical neuronal cytoskeletal changes associated with FIV infection. J Neuro-Oncol 3:283– 289
50. Jones GJ, Barsby NL, Cohen EA, Holden J, Harris K, Dickie P, Jhamandas J, Power C (2007) HIV-1 Vpr causes neuronal apoptosis and in vivo neurodegeneration. J Neurosci 27:3703–3711
51. Joseph J (2015) Eradication of HIV-1 from CNS reservoirs: current strategies and future priorities. J Neuro-Oncol 21:219–221
52. Kang YJ, Digicaylioglu M, Russo R, Kaul M, Achim CL, Fletcher L, Masliah E, Lipton SA (2010) Erythropoietin plus insulin-like growth factor-I protects against neuronal damage in a murine model of human immunodeficiency virus-associated neurocognitive disorders. Ann Neurol 68:342–352
53. Kapadia F, Vlahov D, Donahoe RM, Friedland G (2005) The role of substance abuse in HIV disease progression: reconciling differences from laboratory and epidemiologic investigations. Clin Infect Dis 41:1027–1034
54. Kaul M (2008) HIV’s double strike at the brain: neuronal toxicity and compromised neurogenesis. Front Biosci 13:2484–2494
55. Kaul M, Garden GA, Lipton SA (2001) Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature 410:988–994
56. Kaul M, Ma Q, Medders KE, Desai MK, Lipton SA (2007) HIV-1 coreceptors CCR5 and CXCR4 both mediate neuronal cell death but CCR5 paradoxically can also contribute to protection. Cell Death Differ 14:296–305
57. Keele BF, Jones JH, Terio KA, Estes JD, Rudicell RS, Wilson ML, Li Y, Learn GH, Beasley TM, Schumacher-Stankey J, Wroblewski E, Mosser A, Raphael J, Kamenya S, Lonsdorf EV, Travis DA, Mlengeya T, Kinsel MJ, Else JG, Silvestri G, Goodall J, Sharp PM, Shaw GM, Pusey AE, Hahn BH (2009) Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz. Nature 460:515–519
58. Keppler OT, Welte FJ, Ngo TA, Chin PS, Patton KS, Tsou CL, Abbey NW, Sharkey ME, Grant RM, You Y, Scarborough JD, Ellmeier W, Littman DR, Stevenson M, Charo IF, Herndier BG, Speck RF, Goldsmith MA (2002) Progress toward a human CD4/CCR5 transgenic rat model for de novo infection by human immunodeficiency virus type 1. J Exp Med 195:719–736
59. Kesby JP, Heaton RK, Young JW, Umlauf A, Woods SP, Letendre SL, Markou A, Grant I, Semenova S (2015a) Methamphetamine exposure combined with HIV-1 disease or gp120 expression: comparison of learning and executive functions in humans and mice. Neuropsychopharmacology 40:1899–1909
60. Kesby JP, Hubbard DT, Markou A, Semenova S (2014). Expression of HIV gp120 protein increases sensitivity to the rewarding properties of methamphetamine in mice. Addict Biol 19:593–605
61. Kesby JP, Markou A, Semenova S, Translational Methamphetamine ARCG (2015b) Cognitive deficits associated with combined HIV gp120 expression and chronic methamphetamine exposure in mice. Eur Neuropsychopharmacol 25:141–150
62. Keswani SC, Jack C, Zhou C, Hoke A (2006) Establishment of a rodent model of HIV-associated sensory neuropathy. J Neurosci 26:10299– 10304
63. Kim BO, Liu Y, Ruan Y, ZC X, Schantz L, He JJ (2003) Neuropathologies in transgenic mice expressing human immunodeficiency virus type 1 Tat protein under the regulation of the astrocyte-specific glial fibrillary acidic protein promoter and doxycycline. Am J Pathol 162:1693–1707
64. Kitai R, Zhao ML, Zhang N, Hua LL, Lee SC (2000) Role of MIP-1beta and RANTES in HIV-1 infection of microglia: inhibition of infection and induction by IFNbeta. J Neuroimmunol 110:230–239
65. Klotman PE, Notkins AL (1996) Transgenic models of human immunodeficiency virus type-1. Curr Top Microbiol Immunol 206:197–222
66. 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
67. Krathwohl MD, Kaiser JL (2004) HIV-1 promotes quiescence in human neural progenitor cells. J Infect Dis 190:216–226
68. Krucker T, Toggas SM, Mucke L, Siggins GR (1998) Transgenic mice with cerebral expression of human immunodeficiency virus type-1 coat protein gp120 show divergent changes in short-and long-term potentiation in CA1 hippocampus. Neuroscience 83:691–700
69. Lambotte O, Deiva K, Tardieu M (2003) HIV-1 persistence, viral reservoir, and the central nervous system in the HAART era. Brain Pathol 13:95–103
70. Lawrence DM, Durham LC, Schwartz L, Seth P, Maric D, Major EO (2004) Human immunodeficiency virus type 1 infection of human brain-derived progenitor cells. J Virol 78:7319–7328
71. Lee MH, Amin ND, Venkatesan A, Wang T, Tyagi R, Pant HC, Nath A (2013) Impaired neurogenesis and neurite outgrowth in an HIV-gp120 transgenic model is reversed by exercise via BDNF production and Cdk5 regulation. J Neuro-Oncol 19:418–431
72. Lee MH, Wang T, Jang MH, Steiner J, Haughey N, Ming GL, Song H, Nath A, Venkatesan A (2011) Rescue of adult hippocampal neurogenesis in a mouse model of HIV neurologic disease. Neurobiol Dis 41:678–687
73. Leonard JM, Abramczuk JW, Pezen DS, Rutledge R, Belcher JH, Hakim F, Shearer G, Lamperth L, Travis W, Fredrickson T (1988) Development of disease and virus recovery in transgenic mice containing HIV proviral DNA. Science 242:1665–1670
74. Limoges J, Persidsky Y, Poluektova L, Rasmussen J, Ratanasuwan W, Zelivyanskaya M, McClernon DR, Lanier ER, Gendelman HE (2000) Evaluation of antiretroviral drug efficacy for HIV-1 encephalitis in SCID mice. Neurology 54:379–389
75. Lindl KA, Marks DR, Kolson DL, Jordan-Sciutto KL (2010) HIV-associated neurocognitive disorder: pathogenesis and therapeutic opportunities. J NeuroImmune Pharmacol 5:294–309
76. Marshall DC, Wyss-Coray T, Abraham CR (1998) Induction of matrix metalloproteinase-2 in human immunodeficiency virus-1 glycoprotein 120 transgenic mouse brains. Neurosci Lett 254:97–100
77. Masliah E, Westland CE, Rockenstein EM, Abraham CR, Mallory M, Veinberg I, Sheldon E, Mucke L (1997) Amyloid precursor proteins protect neurons of transgenic mice against acute and chronic excitotoxic injuries in vivo. Neuroscience 78:135–146
78. Mattson MP, Haughey NJ, Nath A (2005) Cell death in HIV dementia. Cell Death Differ 12(Suppl 1):893–904
79. Maung R, Hoefer MM, Sanchez AB, Sejbuk NE, Medders KE, Desai MK, Catalan IC, Dowling CC, de Rozieres CM, Garden GA, Russo R, Roberts AJ, Williams R, Kaul M (2014) CCR5 knockout prevents neuronal injury and behavioral impairment induced in a transgenic mouse model by a CXCR4-using HIV-1 glycoprotein 120. J Immunol 193:1895–1910
80. Meeker RB, Thiede BA, Hall C, English R, Tompkins M (1997) Cortical cell loss in asymptomatic cats experimentally infected with feline immunodeficiency virus. AIDS Res Hum Retrovir 13:1131–1140
81. Melendez RI, Roman C, Capo-Velez CM, Lasalde-Dominicci JA (2016) Decreased glial and synaptic glutamate uptake in the striatum of HIV-1 gp120 transgenic mice. J Neuro-Oncol 22:358–365
82. Minassian A, Henry BL, Woods SP, Vaida F, Grant I, Geyer MA, Perry W, Translational Methamphetamine ARCG (2013) Prepulse inhibition in HIV-associated neurocognitive disorders. J Int Neuropsychol Soc 19:709–717
83. Mitchell SJ, Morris SR, Kent CK, Stansell J, Klausner JD (2006) Methamphetamine use and sexual activity among HIV-infected patients in care—San Francisco, 2004. AIDS Patient Care STDs 20: 502–510
84. Mucke L, Abraham CR, Ruppe MD, Rockenstein EM, Toggas SM, Mallory M, Alford M, Masliah E (1995) Protection against HIV-1 gp120-induced brain damage by neuronal expression of human amyloid precursor protein. J Exp Med 181:1551–1556
85. Nakanishi N, Kang YJ, Tu S, McKercher SR, Masliah E, Lipton SA (2016) Differential effects of pharmacologic and genetic modulation of NMDA receptor activity on HIV/gp120-induced neuronal damage in an in vivo mouse model. J Mol Neurosci 58:59–65
86. Nath A (2015) Eradication of human immunodeficiency virus from brain reservoirs. J Neuro-Oncol 21:227–234
87. Nath BM, Schumann KE, Boyer JD (2000) The chimpanzee and other non-human-primate models in HIV-1 vaccine research. Trends Microbiol 8:426–431
88. Okamoto S, Kang YJ, Brechtel CW, Siviglia E, Russo R, Clemente A, Harrop A, McKercher S, Kaul M, Lipton SA (2007) HIV/gp120 decreases adult neural progenitor cell proliferation via checkpoint kinase-mediated cell-cycle withdrawal and G1 arrest. Cell Stem Cell 1:230–236
89. Okamoto S, Pouladi MA, Talantova M, Yao D, Xia P, Ehrnhoefer DE, Zaidi R, Clemente A, Kaul M, Graham RK, Zhang D, Vincent Chen HS, Tong G, Hayden MR, Lipton SA (2009) Balance between synaptic versus extrasynaptic NMDA receptor activity influences inclusions and neurotoxicity of mutant huntingtin. Nat Med 15:1407– 1413
90. Olmsted RA, Barnes AK, Yamamoto JK, Hirsch VM, Purcell RH, Johnson PR (1989) Molecular cloning of feline immunodeficiency virus. Proc Natl Acad Sci U S A 86:2448–2452
91. Patrick C, Crews L, Desplats P, Dumaop W, Rockenstein E, Achim CL, Everall IP, Masliah E (2011) Increased CDK5 expression in HIV encephalitis contributes to neurodegeneration via tau phosphorylation and is reversed with roscovitine. Am J Pathol 178:1646–1661
92. Perry W, Minassian A, Paulus MP, Young JW, Kincaid MJ, Ferguson EJ, Henry BL, Zhuang X, Masten VL, Sharp RF, Geyer MA (2009) A reverse-translational study of dysfunctional exploration in psychiatric disorders: from mice to men. Arch Gen Psychiatry 66:1072– 1080
93. Persidsky Y, Limoges J, McComb R, Bock P, Baldwin T, Tyor W, Patil A, Nottet HS, Epstein L, Gelbard H, Flanagan E, Reinhard J, Pirruccello SJ, Gendelman HE (1996) Human immunodeficiency virus encephalitis in SCID mice. Am J Pathol 149:1027–1053
94. Petito CK, Roberts B (1995) Evidence of apoptotic cell death in HIV encephalitis. Am J Pathol 146:1121–1130
95. Poli G, Biswas P, Fauci AS (1994) Interferons in the pathogenesis and treatment of human immunodeficiency virus infection. Antivir Res 24:221–233
96. Poluektova L, Meyer V, Walters L, Paez X, Gendelman HE (2005) Macrophage-induced inflammation affects hippocampal plasticity and neuronal development in a murine model of HIV-1 encephalitis. Glia 52:344–353
97. Poluektova LY, Munn DH, Persidsky Y, Gendelman HE (2002) Generation of cytotoxic T cells against virus-infected human brain macrophages in a murine model of HIV-1 encephalitis. J Immunol 168:3941–3949
98. Potash MJ, Chao W, Bentsman G, Paris N, Saini M, Nitkiewicz J, Belem P, Sharer L, Brooks AI, Volsky DJ (2005) A mouse model for study of systemic HIV-1 infection, antiviral immune responses, and neuroinvasiveness. Proc Natl Acad Sci U S A 102:3760–3765
99. Raber J, Toggas SM, Lee S, Bloom FE, Epstein CJ, Mucke L (1996) Central nervous system expression of HIV-1 Gp120 activates the hypothalamic-pituitary-adrenal axis: evidence for involvement of NMDA receptors and nitric oxide synthase. Virology 226:362–373
100. Reid W, Sadowska M, Denaro F, Rao S, Foulke J Jr, Hayes N, Jones O, Doodnauth D, Davis H, Sill A, O'Driscoll P, Huso D, Fouts T, Lewis G, Hill M, Kamin-Lewis R, Wei C, Ray P, Gallo RC, Reitz M, Bryant J (2001) An HIV-1 transgenic rat that develops HIV-related pathology and immunologic dysfunction. Proc Natl Acad Sci U S A 98:9271–9276
101. Roberts AJ, Maung R, Sejbuk NE, Ake C, Kaul M (2010) Alteration of methamphetamine-induced stereotypic behaviour in transgenic mice expressing HIV-1 envelope protein gp120. J Neurosci Methods 186: 222–225
102. Sas AR, Bimonte-Nelson H, Smothers CT, Woodward J, Tyor WR (2009) Interferon-alpha causes neuronal dysfunction in encephalitis. J Neurosci 29:3948–3955
103. Sas AR, Bimonte-Nelson HA, Tyor WR (2007) Cognitive dysfunction in HIV encephalitic SCID mice correlates with levels of interferon-alpha in the brain. AIDS 21:2151–2159
104. Schifitto G, Navia BA, Yiannoutsos CT, Marra CM, Chang L, Ernst T, Jarvik JG, Miller EN, Singer EJ, Ellis RJ, Kolson DL, Simpson D, Nath A, Berger J, Shriver SL, Millar LL, Colquhoun D, Lenkinski R, Gonzalez RG, Lipton SA (2007) Memantine and HIV-associated cognitive impairment: a neuropsychological and proton magnetic resonance spectroscopy study. AIDS 21:1877–1886
105. Schwartz L, Major EO (2006) Neural progenitors and HIV-1-associated central nervous system disease in adults and children. Curr HIV Res 4:319–327
106. Shi B, De GU, He J, Wang S, Lorenzo A, Busciglio J, Gabuzda D (1996) Apoptosis induced by HIV-1 infection of the central nervous system. J Clin Invest 98:1979–1990
107. Soontornniyomkij V, Kesby JP, Morgan EE, Bischoff-Grethe A, Minassian A, Brown GG, Grant I, Translational Methamphetamine ARCG (2016) Effects of HIV and methamphetamine on brain and behavior: evidence from human studies and animal models. J NeuroImmune Pharmacol 11:495–510
108. Steiner JP, Bachani M, Wolfson-Stofko B, Lee MH, Wang T, Li G, Li W, Strayer D, Haughey NJ, Nath A (2015) Interaction of paroxetine with mitochondrial proteins mediates neuroprotection. Neurotherapeutics 12:200–216
109. Thaney VE, O’Neill AM, Hoefer MM, Maung R, Sanchez AB, Kaul M (2017) IFNβ protects neurons from damage in a murine model of HIV-1 associated brain injury. Sci Rep 7:46514
110. Thomas FP, Chalk C, Lalonde R, Robitaille Y, Jolicoeur P (1994) Expression of human immunodeficiency virus type 1 in the nervous system of transgenic mice leads to neurological disease. J Virol 68: 7099–7107
111. Toggas SM, Masliah E, Mucke L (1996) Prevention of HIV-1 gp120-induced neuronal damage in the central nervous system of transgenic mice by the NMDA receptor antagonist memantine. Brain Res 706:303–307
112. Toggas SM, Masliah E, Rockenstein EM, Rall GF, Abraham CR, Mucke L (1994) Central nervous system damage produced by expression of the HIV-1 coat protein gp120 in transgenic mice. Nature 367:188– 193
113. Toggas SM, Mucke L (1996) Transgenic models in the study of AIDS dementia complex. Curr Top Microbiol Immunol 206:223–241
114. Toggas SM, Mucke L (1998) Transgenic models to assess the pathogenic potential of viral products in HIV-1-associated CNS disease. In: Lipton SA, Epstein L, Swindells S (eds) The neurology of AIDS. Gendelman HE. Chapman & Hall, New York, pp 156–167
115. Toneatto S, Finco O, van der PH, Abrignani S, Annunziata P (1999) Evidence of blood-brain barrier alteration and activation in HIV-1 gp120 transgenic mice. AIDS 13:2343–2348
116. Tran PB, Ren D, Miller RJ (2005) The HIV-1 coat protein gp120 regulates CXCR4-mediated signaling in neural progenitor cells. J Neuroimmunol 160:68–76
117. Tyor WR, Power C, Gendelman HE, Markham RB (1993) A model of human immunodeficiency virus encephalitis in SCID mice. Proc Natl Acad Sci U S A 90:8658–8662
118. Urbina A, Jones K (2004) Crystal methamphetamine, its analogues, and HIV infection: medical and psychiatric aspects of a new epidemic. Clin Infect Dis 38:890–894
119. Van Duyne R, Pedati C, Guendel I, Carpio L, Kehn-Hall K, Saifuddin M, Kashanchi F (2009) The utilization of humanized mouse models for the study of human retroviral infections. Retrovirology 6:76
120. Wang EJ, Sun J, Pettoello-Mantovani M, Anderson CM, Osiecki K, Zhao ML, Lopez L, Lee SC, Berman JW, Goldstein H (2003) Microglia from mice transgenic for a provirus encoding a monocyte-tropic HIV type 1 isolate produce infectious virus and display in vitro and in vivo upregulation of lipopolysaccharide-induced chemokine gene expression. AIDS Res Hum Retrovir 19:755–765
121. Wang RG, Kaul M, Zhang DX (2012) Interferon-stimulated gene 15 as a general marker for acute and chronic neuronal injuries. Sheng Li Xue Bao 64:577–583
122. Williams R, Bokhari S, Silverstein P, Pinson D, Kumar A, Buch S (2008) Nonhuman primate models of neuroAIDS. J Neuro-Oncol 14:292– 300
123. Wilson ME, Dimayuga FO, Reed JL, Curry TE, Anderson CF, Nath A, Bruce-Keller AJ (2006) Immune modulation by estrogens: role in CNS HIV-1 infection. Endocrine 29:289–297
124. Wrasidlo W, Crews LA, Tsigelny IF, Stocking E, Kouznetsova VL, Price D, Paulino A, Gonzales T, Overk CR, Patrick C, Rockenstein E, Masliah E (2014) Neuroprotective effects of the anti-cancer drug sunitinib in models of HIV neurotoxicity suggests potential for the treatment of neurodegenerative disorders. Br J Pharmacol 171: 5757–5773
125. Wyss-Coray T, Masliah E, Toggas SM, Rockenstein EM, Brooker MJ, Lee HS, Mucke L (1996) Dysregulation of signal transduction pathways as a potential mechanism of nervous system alterations in HIV-1 gp120 transgenic mice and humans with HIV-1 encephalitis. J Clin Invest 97:789–798
126. Xiang J, George SL, Wunschmann S, Chang Q, Klinzman D, Stapleton JT (2004) Inhibition of HIV-1 replication by GB virus C infection through increases in RANTES, MIP-1alpha, MIP-1beta, and SDF-1. Lancet 363:2040–2046
127. Young JW, Minassian A, Geyer MA (2016) Locomotor profiling from rodents to the clinic and back again. Curr Top Behav Neurosci 28: 287–303
128. Zhou D, Masliah E, Spector SA (2011) Autophagy is increased in postmortem brains of persons with HIV-1-associated encephalitis. J Infect Dis 203:1647–1657