HIV-1 protein gp120 rapidly impairs memory in chicks by interrupting the glutamate-glutamine cycle

Neurobiology of Learning and Memory

Volumn 87, Issue 1, 2007, Pages 1-8

  Fernandes, S P ^a   Edwards, T M ^a   Ng, K T ^a   Robinson, S R ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

AIDS Dementia Complex; Astrocyte; Chick; Glutamate; Glutamine synthetase; Passive avoidance

Indexed keywords

GLUTAMIC ACID; GLUTAMINE; GLYCOPROTEIN GP 120; VIRUS PROTEIN;

AMINO ACID SYNTHESIS; AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; BRAIN REGION; CHICK; CONTROLLED STUDY; EXTRACELLULAR SPACE; HUMAN IMMUNODEFICIENCY VIRUS 1; MEMORY CONSOLIDATION; MEMORY DISORDER; NONHUMAN; PASSIVE AVOIDANCE; PROTEIN TARGETING; PROTEIN TRANSPORT; TASK PERFORMANCE;

AMNESIA; ANIMALS; ASTROCYTES; AVOIDANCE LEARNING; BIOLOGICAL TRANSPORT, ACTIVE; CHICKENS; DOSE-RESPONSE RELATIONSHIP, DRUG; GLUTAMIC ACID; GLUTAMINE; HIV ENVELOPE PROTEIN GP120; HIV-1; MALE; TELENCEPHALON;

EID: 33750514798     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2006.03.006     Document Type: Article

References (46)

1. Bagasra O., Lavi E., Bobroski L., Khalili K., Pestaner J., Tawadros R., et al. Cellular reservoirs of HIV-1 in the central nervous system of infected individuals: identification by the combination of in situ polymerase chain reaction and immunohistochemistry. AIDS 10 6 (1996) 573-585
2. Barnett N.L., Pow D.V., and Robinson S.R. Inhibition of Muller cell glutamine synthetase rapidly impairs the retinal response to light. Glia 30 1 (2000) 64-73
3. Benos D.J., McPherson S., Hahn B.H., Chaikin M.A., and Benveniste E.N. Cytokines and HIV envelope glycoprotein gp120 stimulate Na+/H+ exchange in astrocytes. Journal of Biological Chemistry 269 19 (1994) 13811-13816
4. Brenneman D.E., Westbrook G.L., Fitzgerald S.P., Ennist D.L., Elkins K.L., Ruff M.R., et al. Neuronal cell killing by the envelope protein of HIV and its prevention by vasoactive intestinal peptide. Nature 335 6191 (1988) 639-642
5. Cherkin A. Failure to transfer memory by feeding trained brains to naive chicks. Journal of Biological Psychology 12 1 (1970) 83-85
6. Corasaniti M.T., Bagetta G., Rotiroti D., and Nistico G. The HIV envelope protein gp120 in the nervous system: interactions with nitric oxide, interleukin-1beta and nerve growth factor signalling, with pathological implications in vivo and in vitro. Biochemical Pharmacology 56 2 (1998) 153-156
7. Dawson T.M., and Dawson V.L. gp120 neurotoxicity in primary cortical cultures. Advances in Neuroimmunology 4 3 (1994) 167-173
8. De Vaus J.E., Gibbs M.E., and Ng K.T. Effects of social isolation on memory formation. Behavioural and Neural Biology 29 4 (1980) 473-480
9. Douen A.G., Akiyama K., Hogan M.J., Wang F., Dong L., Chow A.K., et al. Preconditioning with cortical spreading depression decreases intraischemic cerebral glutamate levels and down-regulates excitatory amino acid transporters EAAT1 and EAAT2 from rat cerebal cortex plasma membranes. Journal of Neurochemistry 75 2 (2000) 812-818
10. Ernst T., Chang L., and Arnold S. Increased glial metabolites predict increased working memory network activation in HIV brain injury. Neuroimage 19 4 (2003) 1686-1693
11. Ferrando S.J., Rabkin J.G., van Gorp W., Lin S.H., and McElhiney M. Longitudinal improvement in psychomotor processing speed is associated with potent combination antiretroviral therapy in HIV-1 infection. Journal of Neuropsychiatry and Clinical Neuroscience 15 2 (2003) 208-214
12. Galicia O., Sanchez-Alavez M., Diaz-Ruiz O., Sanchez Narvaez F., Elder J.H., Navarro L., et al. HIV-derived protein gp120 suppresses P3 potential in rats: potential implications in HIV-associated dementia. Neuroreport 1 6 (2000) 1351-1355
13. Garden G.A., Guo W., Jayadev S., Tun C., Balcaitis S., Choi J., et al. HIV associated neurodegeneration requires p53 in neurons and microglia. The FASEB Journal 18 10 (2004) 1141-1143
14. Gemignani A., Paudice P., Pittaluga A., and Raiteri M. The HIV-1 coat protein gp120 and some of its fragments potently activate native cerebral NMDA receptors mediating neuropeptide release. European Journal of Neuroscience 12 8 (2000) 2839-2846
15. Gibbs M.E., Hertz L., and Ng K.T. Inhibition of short-term memory formation in the chick by blockade of extracellular glutamate uptake. Neurobiology of Learning and Memory 81 2 (2004) 115-119
16. Gibbs M.E., and Ng K.T. Psychobiology of memory: towards a model of memory formation. Neuroscience and Biobehavioral Reviews 1 2 (1977) 113-136
17. Gibbs M.E., O'Dowd B.S., Hertz L., Robinson S.R., Sedman G.L., and Ng K.T. Inhibition of glutamine synthetase activity prevents memory consolidation. Cognitive Brain Research 4 1 (1996) 57-64
18. Glowa J.R., Panlilio L.V., Brenneman D.E., Gozes I., Fridkin M., and Hill J.M. Learning impairment following intracerebral administration of the HIV envelope protein gp120 or a VIP antagonist. Brain Research 570 1-2 (1992) 49-53
19. Hertz L., Dringen R., Schousboe A., and Robinson S.R. Astrocytes: glutamate producers for neurons. Journal of Neuroscience Research 57 4 (1999) 417-428
20. Holden C.P., Haughey N.J., Nath A., and Geiger J.D. Role of Na+/H+ exchangers, excitatory amino acid receptors and voltage-operated Ca2+ channels in human immunodeficiency virus type 1 gp120-mediated increases in intracellular Ca2+ in human neurons and astrocytes. Neuroscience 91 4 (1999) 1369-1378
21. Kanmogne G.D., Kennedy R.C., and Grammas P. HIV-1 gp120 proteins and gp160 peptides are toxic to brain endothelial cells and neurons: possible pathway for HIV entry into the brain and HIV-associated dementia. Journal of Neuropathology and Experimental Neurology 61 11 (2002) 992-1000
22. Korbo L., and West M. No loss of hippocampal neurons in AIDS patients. Acta Neuropatholologica (Berl) 99 5 (2000) 529-533
23. Lipton S.A., Sucher N.J., Kaiser P.K., and Dreyer E.B. Synergistic effects of HIV coat protein and NMDA receptor-mediated neurotoxicity. Neuron 7 1 (1991) 111-118
24. Navia B.A., Jordan B.D., and Price R.W. The AIDS dementia complex: I. Clinical features. Annals of Neurology 19 6 (1986) 517-524
25. Ng K.T., O'Dowd B.S., Rickard N.S., Robinson S.R., Gibbs M.E., Rainey C., et al. Complex roles of glutamate in the Gibbs-Ng model of one-trial aversive learning in the new-born chick. Neuroscience and Biobehavioural Reviews 21 1 (1997) 45-54
26. Norenberg M.D., and Martinez-Hernandez A. Fine structural localization of glutamine synthetase in astrocytes of rat brain. Brain Research 161 2 (1979) 303-310
27. Noyer C.M., Simon D., Borczuk A., Brandt L.J., Lee M.J., and Nehra V. A double-blind placebo-controlled pilot study of glutamine therapy for abnormal intestinal permeability in patients with AIDS. American Journal of Gastroenterology 93 6 (1998) 972-975
28. Nuovo G.J., Becker J., Burk M.W., Margiotta M., Fuhrer J., and Steigbigel R.T. In situ detection of PCR-amplified HIV-1 nucleic acids in lymph nodes and peripheral blood in patients with asymptomatic HIV-1 infection and advanced-stage AIDS. Journal of Acquired Immune Deficiency Syndrome 7 9 (1994) 916-923
29. Patton H.K., Zhou Z.H., Bubien J.K., Benveniste E.N., and Benos D.J. gp120-induced alterations of human astrocyte function: Na(+)/H(+) exchange, K(+) conductance, and glutamate flux. American Journal of Physiology and Cell Physiology 279 3 (2000) C700-C708
30. Pow D.V., and Robinson S.R. Glutamate in some retinal neurons is derived solely from glia. Neuroscience 60 2 (1994) 355-366
31. Pugh C.R., Johnson J.D., Martin D., Rudy J.W., Maier S.F., and Watkins L.R. Human immunodeficiency virus-1 coat protein gp120 impairs contextual fear conditioning: a potential role in AIDS related learning and memory impairments. Brain Research 861 1 (2000) 8-15
32. Reger M., Welsh R., Razani J., Martin D.J., and Boone K.B. A meta-analysis of the neuropsychological sequelae of HIV infection. Journal of the International Neuropsychological Society 8 3 (2002) 410-424
33. Rickard N.S., Poot A.C., Gibbs M.E., and Ng K.T. Both non-NMDA and NMDA glutamate receptors are necessary for memory consolidation in the day-old chick. Behavioral and Neural Biology 62 1 (1994) 33-40
34. Rose S.P., and Csillag A. Passive avoidance training results in lasting changes in deoxyglucose metabolism in left hemisphere regions of chick brain. Behavioral and Neural Biology 44 2 (1985) 315-324
35. Sanchez-Alavez M., Criado J., Gomez-Chavarin M., Jimenez-Anguiano A., Navarro L., Diaz-Ruiz O., et al. HIV- and FIV-derived gp120 alter spatial memory, LTP, and sleep in rats. Neurobiology of Disease 7 4 (2000) 384-394
36. Shabert J.K., Winslow C., Lacey J.M., and Wilmore D.W. Glutamine-antioxidant supplementation increases body cell mass in AIDS patients with weight loss: a randomized, double-blind controlled trial. Nutrition 15 11-12 (1999) 860-864
37. Suchak S.K., Baloyianni N.V., Perkinton M.S., Williams R.J., Meldrum B.S., and Rattray M. The 'glial' glutamate transporter, EAAT2 (Glt-1) accounts for high affinity glutamate uptake into adult rodent nerve endings. Journal of Neurochemistry 84 3 (2003) 522-532
38. Tardieu M. HIV-1-related central nervous system diseases. Current Opinion in Neurology 12 4 (1999) 377-381
39. Tozzi V., Balestra P., Galgani S., Narciso P., Ferri F., Sebastiani G., et al. Positive and sustained effects of highly active antiretroviral therapy on HIV-1-associated neurocognitive impairment. AIDS 13 14 (1999) 1889-1897
40. Tozzi V., Balestra P., Galgani S., Narciso P., Sampaolesi A., Antinori A., et al. Changes in neurocognitive performance in a cohort of patients treated with HAART for 3 years. Journal of Acquired Immune Deficiency Syndrome 28 1 (2001) 19-27
41. Turecek R., and Trussell L.O. Control of synaptic depression by glutamate transporters. Journal of Neuroscience 20 5 (2000) 2054-2063
42. Vesce S., Bezzi P., Rossi D., Meldolesi J., and Volterra A. HIV-1 gp120 glycoprotein affects the astrocyte control of extracellular glutamate by both inhibiting the uptake and stimulating the release of the amino acid. FEBS Letters 411 1 (1997) 107-109
43. Vorwerk C.K., Naskar R., Schuettauf F., Quinto K., Zurakowski D., Gochenauer G., et al. Depression of retinal glutamate transporter function leads to elevated intravitreal glutamate levels and ganglion cell death. Investigative Ophthalmology and Visual Science 41 11 (2000) 3615-3621
44. Wang Z., Pekarskaya O., Bencheikh M., Chao W., Gelbard H.A., Ghorpade A., et al. Reduced expression of glutamate transporter EAAT2 and impaired glutamate transport in human primary astrocytes exposed to HIV-1 or gp120. Virology 312 1 (2003) 60-73
45. Wang Z., Trillo-Pazos G., Kim S.Y., Canki M., Morgello S., Sharer L.R., et al. Effects of human immunodeficiency virus type 1 on astrocyte gene expression and function: potential role in neuropathogenesis. Journal of Neurovirology 10 Suppl. 1 (2004) 25-32
46. Wang Y.S., and White T.D. The HIV glycoproteins gp41 and gp120 cause rapid excitation in rat cortical slices. Neuroscience Letters 291 1 (2000) 13-16