Rodent models for HIV-associated neurocognitive disorders

Trends in Neurosciences

Volumn 35, Issue 3, 2012, Pages 197-208

  Gorantla, Santhi ^a   Poluektova, Larisa ^a   Gendelman, Howard E ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Cognitive impairment; HIV associated neurocognitive disorders; Human immunodeficiency virus type one; Neuroinflammation; Rodent model

Indexed keywords

CD34 ANTIGEN; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR4; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA;

ANTIVIRAL THERAPY; ASTROCYTE; BLOOD BRAIN BARRIER; BONE MARROW; CD4+ T LYMPHOCYTE; CYTOKINE PRODUCTION; DISEASE MODEL; HIV ASSOCIATED DEMENTIA; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE DEFICIENCY; LENTIVIRINAE; LYMPHOCYTE; MACROPHAGE; MONOCYTE; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROVIRUS; REGULATORY T LYMPHOCYTE; REVIEW; TRANSGENIC ANIMAL; VIRUS MORPHOLOGY; VIRUS REPLICATION;

AIDS DEMENTIA COMPLEX; ANIMALS; ANTI-HIV AGENTS; BLOOD-BRAIN BARRIER; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; HIV INFECTIONS; HIV-1; HUMANS; LENTIVIRUS INFECTIONS; RODENTIA;

EID: 84857690625     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2011.12.006     Document Type: Review

References (123)

1. Heaton R.K., et al. HIV-associated neurocognitive disorders before and during the era of combination antiretroviral therapy: differences in rates, nature, and predictors. J. Neurovirol. 2011, 17:3-16.
2. Antinori A., et al. Updated research nosology for HIV-associated neurocognitive disorders. Neurology 2007, 69:1789-1799.
3. Woods S.P., et al. Cognitive neuropsychology of HIV-associated neurocognitive disorders. Neuropsychol. Rev. 2009, 19:152-168.
4. Lanoy E., et al. Survival after neuroAIDS: association with antiretroviral CNS Penetration-Effectiveness score. Neurology 2011, 76:644-651.
5. Masliah E., et al. Changes in pathological findings at autopsy in AIDS cases for the last 15 years. Aids 2000, 14:69-74.
6. Kraft-Terry S.D., et al. A coat of many colors: neuroimmune crosstalk in human immunodeficiency virus infection. Neuron 2009, 64:133-145.
7. Kaul M. HIV-1 associated dementia: update on pathological mechanisms and therapeutic approaches. Curr. Opin. Neurol. 2009, 22:315-320.
8. Van Duyne R., et al. The utilization of humanized mouse models for the study of human retroviral infections. Retrovirology 2009, 6:76.
9. Garcia-Arriaza J., et al. Immunogenic profiling in mice of a HIV/AIDS vaccine candidate (MVA-B) expressing four HIV-1 antigens and potentiation by specific gene deletions. PLoS ONE 2010, 5.
10. Feldman C. Pneumonia associated with HIV infection. Curr. Opin. Infect. Dis. 2005, 18:165-170.
11. Obrecht R.E., Patrick P.D. Neuropsychological sequelae of adolescent infectious diseases. Adolesc. Med. 2002, 13:663-681.
12. Kennedy P.G., et al. Persistent expression of Ia antigen and viral genome in visna-maedi virus-induced inflammatory cells. Possible role of lentivirus-induced interferon. J. Exp. Med. 1985, 162:1970-1982.
13. Loman D.C. Het Texels schaap. Magazijn voor Landbouw en Kruidkunde II 1862, 66-70.
14. Ligneó M{cyrillic}. Meómoire et observations sur une maladie de sang, connue sous le nom d'anhumie hydrohumie, cachexie acquise du cheval. Reócueil de Meódecine Veóteórinaire, Ecole Alfort 1843, 30-44.
15. Rajya B.S., Singh C.M. The pathology of pneumonia and associated respiratory disease of sheep and goats. I. Occurrence of Jagziekte and Maedi in sheep and goats in India. Am. J. Vet. Res. 1964, 25:61-67.
16. Joag S. Primate models of AIDS. Microbes Infect. 2000, 2:223-229.
17. Gonda M.A., et al. Characterization and molecular cloning of a bovine lentivirus related to human immunodeficiency virus. Nature 1987, 330:388-391.
18. Pedersen N.C., et al. Isolation of a T-lymphotropic virus from domestic cats with an immunodeficiency-like syndrome. Science 1987, 235:790-793.
19. Weiss A. T cell antigen receptor signal transduction: a tale of tails and cytoplasmic protein-tyrosine kinases. Cell 1993, 73:209-212.
20. Narayan O., et al. Visna virus infection of American lambs. Science 1974, 183:1202-1203.
21. Persidsky Y., et al. Rodent model systems for studies of HIV-1 associated dementia. Neurotox. Res. 2005, 8:91-106.
22. Gama Sosa M.A., et al. Animal transgenesis: an overview. Brain Struct. Funct. 2010, 214:91-109.
23. Thomas F.P., et al. Expression of human immunodeficiency virus type 1 in the nervous system of transgenic mice leads to neurological disease. J. Virol. 1994, 68:7099-7107.
24. Santoro T.J., et al. Growth failure and AIDS-like cachexia syndrome in HIV-1 transgenic mice. Virology 1994, 201:147-151.
25. Wang E.J., et al. 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. Retroviruses 2003, 19:755-765.
26. Sun J., et al. Increased in vivo activation of microglia and astrocytes in the brains of mice transgenic for an infectious R5 human immunodeficiency virus type 1 provirus and for CD4-specific expression of human cyclin T1 in response to stimulation by lipopolysaccharides. J. Virol. 2008, 82:5562-5572.
27. Reid W., et al. An HIV-1 transgenic rat that develops HIV-related pathology and immunologic dysfunction. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:9271-9276.
28. Lashomb A.L., et al. Further characterization of the spatial learning deficit in the human immunodeficiency virus-1 transgenic rat. J. Neurovirol. 2009, 15:14-24.
29. Rao J.S., et al. Increased neuroinflammatory and arachidonic acid cascade markers, and reduced synaptic proteins, in brain of HIV-1 transgenic rats. J. Neuroinflammation 2011, 8:101.
30. Kass M.D., et al. Methamphetamine-induced behavioral and physiological effects in adolescent and adult HIV-1 transgenic rats. J. Neuroimmune Pharmacol. 2010, 5:566-573.
31. Li W., et al. Molecular and cellular mechanisms of neuronal cell death in HIV dementia. Neurotox. Res. 2005, 8:119-134.
32. Toggas S.M., et al. Central nervous system damage produced by expression of the HIV-1 coat protein gp120 in transgenic mice. Nature 1994, 367:188-193.
33. Kim B.O., et al. 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. 2003, 162:1693-1707.
34. Garden G.A., et al. Caspase cascades in human immunodeficiency virus-associated neurodegeneration. J. Neurosci. 2002, 22:4015-4024.
35. Toneatto S., et al. Evidence of blood-brain barrier alteration and activation in HIV-1 gp120 transgenic mice. AIDS 1999, 13:2343-2348.
36. Jones G.J., et al. HIV-1 Vpr causes neuronal apoptosis and in vivo neurodegeneration. J. Neurosci. 2007, 27:3703-3711.
37. Power C., et al. Delineating HIV-associated neurocognitive disorders using transgenic models: the neuropathogenic actions of Vpr. J. Neuroimmune Pharmacol. 2011, 10.1007/s11481-011-9310-7.
38. Hanna Z., et al. Nef harbors a major determinant of pathogenicity for an AIDS-like disease induced by HIV-1 in transgenic mice. Cell 1998, 95:163-175.
39. Kurth J., et al. In vivo transcriptional regulation of the human immunodeficiency virus in the central nervous system in transgenic mice. J. Virol. 1996, 70:7686-7694.
40. Andrade A.S., et al. A programmable prompting device improves adherence to highly active antiretroviral therapy in HIV-infected subjects with memory impairment. Clin. Infect. Dis. 2005, 41:875-882.
41. Fu W., et al. Human immunodeficiency virus type 1, human protein interaction database at NCBI. Nucleic Acids Res. 2009, 37:D417-D422.
42. van Dijk D., et al. Identifying potential survival strategies of HIV-1 through virus-host protein interaction networks. BMC Syst. Biol. 2010, 4:96.
43. van Maanen M., Sutton R.E. Rodent models for HIV-1 infection and disease. Curr. HIV Res. 2003, 1:121-130.
44. Zhang L., et al. Current humanized mouse models for studying human immunology and HIV-1 immuno-pathogenesis. Sci. China Life Sci. 2010, 53:195-203.
45. Rosenberg Z.F., Fauci A.S. The immunopathogenesis of HIV infection. Adv. Immunol. 1989, 47:377-431.
46. Zhang J.-X., et al. Relief of preintegration inhibition and characterization of additional blocks for HIV replication in primary mouse T cells. PLoS ONE 2008, 3:e2035.
47. Keppler O., et al. Progress toward a human CD4/CCR5 transgenic rat model for de novo infection by human immunodeficiency virus type 1. J. Exp. Med. 2002, 195:719-736.
48. Goffinet C., et al. HIV-susceptible transgenic rats allow rapid preclinical testing of antiviral compounds targeting virus entry or reverse transcription. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:1015-1020.
49. Paul J.B., et al. Mice transgenic for monocyte-tropic HIV type 1 produce infectious virus and display plasma viremia: a new in vivo system for studying the postintegration phase of HIV replication. AIDS Res. Hum. Retroviruses 2000, 16:481-492.
50. + T cell homeostasis and in vitro HIV-1 susceptibility in transgenic mice expressing T cell line-tropic HIV-1 receptors. J. Exp. Med. 1998, 187:1439-1449.
51. Speck R.F., et al. Rabbit cells expressing human CD4 and human CCR5 are highly permissive for human immunodeficiency virus type 1 infection. J. Virol. 1998, 72:5728-5734.
52. Tervo H., et al. Mouse T-cells restrict replication of human immunodeficiency virus at the level of integration. Retrovirology 2008, 5:58.
53. Nitkiewicz J., et al. Productive infection of primary murine astrocytes, lymphocytes, and macrophages by human immunodeficiency virus type 1 in culture. J. Neurovirol. 2004, 10:400-408.
54. Potash M.J., et al. A mouse model for study of systemic HIV-1 infection, antiviral immune responses, and neuroinvasiveness. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:3760-3765.
55. Hadas E., et al. Testing antiretroviral drug efficacy in conventional mice infected with chimeric HIV-1. AIDS 2007, 21:905-909.
56. + patients protected mice against chimaeric ecotropic HIV-1 challenge. Eur. J. Immunol. 2009, 39:1831-1840.
57. Hinkula J., et al. Genetic immunization with multiple HIV-1 genes provides protection against HIV-1/MuLV pseudovirus challenge in vivo. Cells Tissues Organs 2004, 177:169-184.
58. Gorantla S., et al. Copolymer-1 induces adaptive immune anti-inflammatory glial and neuroprotective responses in a murine model of HIV-1 encephalitis. J. Immunol. 2007, 179:4345-4356.
59. Gorantla S., et al. Modulation of innate immunity by copolymer-1 leads to neuroprotection in murine HIV-1 encephalitis. Glia 2008, 56:223-232.
60. + regulatory T cells in a murine model of HIV-1-associated neurodegeneration. J. Immunol. 2009, 182:3855-3865.
61. Gong N., et al. Brain ingress of regulatory T cells in a murine model of HIV-1 encephalitis. J. Neuroimmunol. 2010, 230:33-41.
62. Tyor W.R., et al. A model of human immunodeficiency virus encephalitis in scid mice. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:8658-8662.
63. Persidsky Y., et al. The development of animal model systems for HIV-1 encephalitis and its associated dementia. J. Neurovirol. 1995, 1:229-243.
64. Poluektova L., et al. Neuroregulatory events follow adaptive immune-mediated elimination of HIV-1-infected macrophages: studies in a murine model of viral encephalitis. J. Immunol. 2004, 172:7610-7617.
65. Zink W.E., et al. Impaired spatial cognition and synaptic potentiation in a murine model of human immunodeficiency virus type 1 encephalitis. J. Neurosci. 2002, 22:2096-2105.
66. Gendelman H.E., et al. Immunopathogenesis of human immunodeficiency virus infection in the central nervous system. Ann. Neurol. 1988, 23:S78-S81.
67. Persidsky Y., et al. Human immunodeficiency virus encephalitis in SCID mice. Am. J. Pathol. 1996, 149:1027-1053.
68. Avgeropoulos N., et al. SCID mice with HIV encephalitis develop behavioral abnormalities. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 1998, 18:13-20.
69. Anderson E.R., et al. Hippocampal synaptic dysfunction in a murine model of human immunodeficiency virus type 1 encephalitis. Neuroscience 2003, 118:359-369.
70. Sas A.R., et al. Interferon-α causes neuronal dysfunction in encephalitis. J. Neurosci. 2009, 29:3948-3955.
71. Xiong H., et al. HIV-1 infected mononuclear phagocyte secretory products affect neuronal physiology leading to cellular demise: relevance for HIV-1-associated dementia. J. Neurovirol. 2000, 6(Suppl. 1):S14-S23.
72. Nukuna A., et al. Levels of human immunodeficiency virus type 1 (HIV-1) replication in macrophages determines the severity of murine HIV-1 encephalitis. J. Neurovirol. 2004, 10(Suppl. 1):82-90.
73. Limoges J., et al. The efficacy of potent anti-retroviral drug combinations tested in a murine model of HIV-1 encephalitis. Virology 2001, 281:21-34.
74. Persidsky Y., et al. Reduction in glial immunity and neuropathology by a PAF antagonist and an MMP and TNFα inhibitor in SCID mice with HIV-1 encephalitis. J. Neuroimmunol. 2001, 114:57-68.
75. Dou H., et al. Neuroprotective mechanisms of lithium in murine human immunodeficiency virus-1 encephalitis. J. Neurosci. 2005, 25:8375-8385.
76. Dou H., et al. Neuroprotective activities of sodium valproate in a murine model of human immunodeficiency virus-1 encephalitis. J. Neurosci. 2003, 23:9162-9170.
77. Dou H., et al. Neuropathologic and neuroinflammatory activities of HIV-1-infected human astrocytes in murine brain. Glia 2006, 54:81-93.
78. Dou H., et al. Macrophage delivery of nanoformulated antiretroviral drug to the brain in a murine model of neuroAIDS. J. Immunol. 2009, 183:661-669.
79. Spitzenberger T.J., et al. Novel delivery system enhances efficacy of antiretroviral therapy in animal model for HIV-1 encephalitis. J. Cereb. Blood Flow Metab. 2007, 27:1033-1042.
80. Poluektova L., et al. Macrophage-induced inflammation affects hippocampal plasticity and neuronal development in a murine model of HIV-1 encephalitis. Glia 2005, 52:344-353.
81. Eggert D., et al. Development of a platelet-activating factor antagonist for HIV-1 associated neurocognitive disorders. J. Neuroimmunol. 2009, 213:47-59.
82. Eggert D., et al. Neuroprotective activities of CEP-1347 in models of neuroAIDS. J. Immunol. 2010, 184:746-756.
83. Limoges J., et al. Dexamethasone therapy worsens the neuropathology of human immunodeficiency virus type 1 encephalitis in SCID mice. J. Infect. Dis. 1997, 175:1368-1381.
84. Munoz-Moreno J.A., et al. Nadir CD4 cell count predicts neurocognitive impairment in HIV-infected patients. AIDS Res. Hum. Retroviruses 2008, 24:1301-1307.
85. + T cells in cerebrospinal fluid compared to those in blood among antiretroviral therapy-naive HIV-positive subjects. J. Virol. 2008, 82:10418-10428.
86. + T-cell infiltrates in human immunodeficiency virus type 1-associated central nervous system disease in children. Clin. Diagn. Lab. Immunol. 1999, 6:105-114.
87. McCrossan M., et al. An immune control model for viral replication in the CNS during presymptomatic HIV infection. Brain 2006, 129:503-516.
88. Poluektova L.Y., et al. Generation of cytotoxic T cells against virus-infected human brain macrophages in a murine model of HIV-1 encephalitis. J. Immunol. 2002, 168:3941-3949.
89. Potula R., et al. Inhibition of indoleamine 2,3-dioxygenase (IDO) enhances elimination of virus-infected macrophages in an animal model of HIV-1 encephalitis. Blood 2005, 106:2382-2390.
90. Gorantla S., et al. Immunoregulation of a CB2 receptor agonist in a murine model of neuroAIDS. J. Neuroimmune Pharmacol. 2010, 5:456-468.
91. Potula R., et al. Peroxisome proliferator-activated receptor-gamma activation suppresses HIV-1 replication in an animal model of encephalitis. Aids 2008, 22:1539-1549.
92. Ito M., et al. NOD/SCID/gamma(c)(null) mouse: an excellent recipient mouse model for engraftment of human cells. Blood 2002, 100:3175-3182.
93. Ishikawa F., et al. Development of functional human blood and immune systems in NOD/SCID/IL2 receptor γ chain(null) mice. Blood 2005, 106:1565-1573.
94. Manz M.G., Di Santo J.P. Renaissance for mouse models of human hematopoiesis and immunobiology. Nat. Immunol. 2009, 10:1039-1042.
95. Watanabe S., et al. Hematopoietic stem cell-engrafted NOD/SCID/IL2Rgamma null mice develop human lymphoid systems and induce long-lasting HIV-1 infection with specific humoral immune responses. Blood 2007, 109:212-218.
96. Brehm M.A., et al. Parameters for establishing humanized mouse models to study human immunity: analysis of human hematopoietic stem cell engraftment in three immunodeficient strains of mice bearing the IL2Rγ null mutation. Clin. Immunol. 2010, 135:84-98.
97. + effector memory T lymphocytes leads to preferential depletion of memory T lymphocytes in R5 HIV-1-infected humanized NOD/SCID/IL-2Rgammanull mice. Virology 2009, 394:64-72.
98. -/-, and C.B-17-scid/bg immunodeficient mice. Hum. Immunol. 2009, 70:790-802.
99. Gorantla S., et al. Links between progressive HIV-1 infection of humanized mice and viral neuropathogenesis. Am. J. Pathol. 2010, 177:2938-2949.
100. Kumar P., et al. T cell-specific siRNA delivery suppresses HIV-1 infection in humanized mice. Cell 2008, 134:577-586.
101. Dash P.K., et al. Loss of neuronal integrity during progressive HIV-1 infection of humanized mice. J. Neurosci. 2011, 31:3148-3157.
102. Williams K., et al. Magnetic resonance spectroscopy reveals that activated monocytes contribute to neuronal injury in SIV neuroAIDS. J. Clin. Invest. 2005, 115:2534-2545.
103. Nowacek A.S., et al. Analyses of nanoformulated antiretroviral drug charge, size, shape and content for uptake, drug release and antiviral activities in human monocyte-derived macrophages. J. Control. Release 2010, 150:204-211.
104. Nowacek A.S., et al. Nanoformulated antiretroviral drug combinations extend drug release and antiretroviral responses in HIV-1-infected macrophages: implications for neuroAIDS therapeutics. J. Neuroimmune Pharmacol. 2010, 5:592-601.
105. Dash P., et al. Safety and efficacy of nanoART in humanized mice. Third Internal Workshop on Humanized Mice 2011, 125.
106. -/- mice. J. Virol. 2007, 81:2700-2712.
107. + cell depletion accelerates HIV-1 immunopathology in humanized mice. J. Immunol. 2010, 184:7082-7091.
108. Bruggeman L.A., Nelson P.J. Controversies in the pathogenesis of HIV-associated renal diseases. Nat. Rev. Nephrol. 2009, 5:574-581.
109. Wang E.-J., et al. 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. Retroviruses 2003, 19:755-765.
110. + T lymphocytes and myeloid cells in mice transgenic for a provirus encoding a monocyte-tropic HIV-1 isolate. J. Virol. 2006, 80:1850-1862.
111. Berrada F., et al. Neuronal expression of human immunodeficiency virus type 1 env proteins in transgenic mice: distribution in the central nervous system and pathological alterations. J. Virol. 1995, 69:6770-6778.
112. Michaud J., et al. Neuropathology of NFHgp160 transgenic mice expressing HIV-1 env protein in neurons. J. Neuropathol. Exp. Neurol. 2001, 60:574-587.
113. Asensio V.C., et al. 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. 2001, 75:7067-7077.
114. Toggas S.M., et al. Prevention of HIV-1 gp120-induced neuronal damage in the central nervous system of transgenic mice by the NMDA receptor antagonist memantine. Brain Res. 1996, 706:303-307.
115. Hauser K.F., et al. HIV-1 Tat and morphine have interactive effects on oligodendrocyte survival and morphology. Glia 2009, 57:194-206.
116. Zou W., et al. Protection against human immunodeficiency virus type 1 Tat neurotoxicity by Ginkgo biloba extract EGb 761 involving glial fibrillary acidic protein. Am. J. Pathol. 2007, 171:1923-1935.
117. Goudreau G., et al. Vacuolar myelopathy in transgenic mice expressing human immunodeficiency virus type 1 proteins under the regulation of the myelin basic protein gene promoter. Nat. Med. 1996, 2:655-661.
118. Radja F., et al. Oligodendrocyte-specific expression of human immunodeficiency virus type 1 Nef in transgenic mice leads to vacuolar myelopathy and alters oligodendrocyte phenotype in vitro. J. Virol. 2003, 77:11745-11753.
119. Noorbakhsh F., et al. MicroRNA profiling reveals new aspects of HIV neurodegeneration: caspase-6 regulates astrocyte survival. FASEB J. 2010, 24:1799-1812.
120. + neurons and human immunodeficiency virus type 1 (HIV-1) regulatory gene expression in the HIV-1 transgenic rat: effects of vitamin A deficiency and morphine. J. Neurovirol. 2010, 16:33-40.
121. Peng H., et al. HIV-1-infected and/or immune activated macrophages regulate astrocyte SDF-1 production through IL-1beta. Glia 2006, 54:619-629.
122. Sas A.R., et al. Cognitive dysfunction in HIV encephalitic SCID mice correlates with levels of Interferon-alpha in the brain. AIDS 2007, 21:2151-2159.
123. Potula R., et al. Alcohol abuse enhances neuroinflammation and impairs immune responses in an animal model of human immunodeficiency virus-1 encephalitis. Am. J. Pathol. 2006, 168:1335-1344.