Mutation of tyrosine 470 of human dopamine transporter is critical for HIV-1 tat-induced inhibition of dopamine transport and transporter conformational transitions

Journal of Neuroimmune Pharmacology

Volumn 8, Issue 4, 2013, Pages 975-987

  Midde, Narasimha M ^a   Huang, Xiaoqin ^b   Gomez, Adrian M ^a   Booze, Rosemarie M ^a   Zhan, Chang Guo ^b   Zhu, Jun ^a  

^a UNIVERSITY OF SOUTH CAROLINA   (United States)

^b University of Kentucky   (United States)

Author keywords

Allosteric modulation; Computational modeling; Dopamine transporter; HIV 1 Tat; Mutation; Uptake

Indexed keywords

COCAINE; DOPAMINE TRANSPORTER; TRANSACTIVATOR PROTEIN; VANOXERINE; ZINC;

ANIMAL CELL; ARTICLE; BINDING SITE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; FEMALE; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SIMULATION; VELOCITY;

ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; DOPAMINE; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; HUMANS; MUTATION; PROTEIN BINDING; PROTEIN CONFORMATION; RATS; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; TYROSINE;

EID: 84882290150     PISSN: 15571890     EISSN: 15571904     Source Type: Journal    
DOI: 10.1007/s11481-013-9464-6     Document Type: Article

References (54)

1. Aksenov MY, Aksenova MV, Mactutus CF, Booze RM (2009) Attenuated neurotoxicity of the transactivation-defective HIV-1 Tat protein in hippocampal cell cultures. Exp Neurol 219:586-590
2. Albini A, Ferrini S, Benelli R, Sforzini S, Giunciuglio D, Aluigi MG, Proudfoot AE, Alouani S, Wells TN, Mariani G, Rabin RL, Farber JM, Noonan DM (1998) HIV-1 Tat protein mimicry of chemokines. Proc Natl Acad Sci U S A 95:13153-13158
3. Andersen PH, Jansen JA, Nielsen EB (1987) [3H]GBR 12935 binding in vivo in mouse brain: Labelling of a piperazine acceptor site. Eur J Pharmacol 144:1-6
4. Berger JR, Arendt G (2000) HIV dementia: The role of the basal ganglia and dopaminergic systems. J Psychopharmacol 14:214-221
5. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
6. Buch S, Yao H, Guo M, Mori T, Su TP, Wang J (2011) Cocaine and HIV-1 interplay: Molecular mechanisms of action and addiction. J Neuroimmune Pharmacol 6:503-515
7. Chang L, Wang GJ, Volkow ND, Ernst T, Telang F, Logan J, Fowler JS (2008) Decreased brain dopamine transporters are related to cognitive deficits in HIV patients with or without cocaine abuse. NeuroImage 42:869-878
8. Chen N, Rickey J, Berfield JL, Reith ME (2004) Aspartate 345 of the dopamine transporter is critical for conformational changes in substrate translocation and cocaine binding. J Biol Chem 279:5508-5519
9. Del Valle L, Croul S, Morgello S, Amini S, Rappaport J, Khalili K (2000) Detection of HIV-1 Tat and JCV capsid protein, VP1, in AIDS brain with progressive multifocal leukoencephalopathy. J Neurovirol 6:221-228
10. Ernst T, Yakupov R, Nakama H, Crocket G, Cole M, Watters M, Ricardo-Dukelow ML, Chang L (2009) Declined neural efficiency in cognitively stable human immunodeficiency virus patients. Ann Neurol 65:316-325
11. Ferris MJ, Mactutus CF, Booze RM (2008) Neurotoxic profiles of HIV, psychostimulant drugs of abuse, and their concerted effect on the brain: Current status of dopamine system vulnerability in NeuroAIDS. Neurosci Biobehav Rev 32:883-909
12. Ferris MJ, Frederick-Duus D, Fadel J, Mactutus CF, Booze RM (2010) Hyperdopaminergic tone in HIV-1 protein treated rats and cocaine sensitization. J Neurochem 115:885-896
13. Gabdoulline RR, Wade RC (1998) Brownian dynamics simulation of protein-protein diffusional encounter. Methods 14:329-341
14. Gannon P, Khan MZ, Kolson DL (2011) Current understanding of HIV-associated neurocognitive disorders pathogenesis. Curr Opin Neurol 24:275-283
15. Gaskill PJ, Calderon TM, Luers AJ, Eugenin EA, Javitch JA, Berman JW (2009) Human immunodeficiency virus (HIV) infection of human macrophages is increased by dopamine: A bridge between HIV-associated neurologic disorders and drug abuse. Am J Pathol 175:1148-1159
16. Gelman BB, Lisinicchia JG, Chen T, Johnson KM, Jennings K, Freeman DH Jr, Soukup VM (2012) Prefrontal dopaminergic and enkephalinergic synaptic accommodation in HIV-associated neurocognitive disorders and encephalitis. J Neuroimmune Pharmacol 7:686-700
17. Guptaroy B, Fraser R, Desai A, Zhang M, Gnegy ME (2011) Site-directed mutations near transmembrane domain 1 alter conformation and function of norepinephrine and dopamine transporters. Mol Pharmacol 79:520-532
18. Guptaroy B, Zhang M, Bowton E, Binda F, Shi L, Weinstein H, Galli A, Javitch JA, Neubig RR, Gnegy ME (2009) A juxtamembrane mutation in the N terminus of the dopamine transporter induces preference for an inward-facing conformation. Mol Pharmacol 75:514-524
19. Harrod SB, Mactutus CF, Fitting S, Hasselrot U, Booze RM (2008) Intra-accumbal Tat1-72 alters acute and sensitized responses to cocaine. Pharmacol Biochem Behav 90:723-729
20. Ho BK, Gruswitz F (2008) HOLLOW: generating accurate representations of channel and interior surfaces in molecular structures. BMC structural biology 8:49.
21. Huang X, Zhan CG (2007) How dopamine transporter interacts with dopamine: Insights from molecular modeling and simulation. Biophys J 93:3627-3639
22. Huang X, Gu HH, Zhan CG (2009) Mechanism for cocaine blocking the transport of dopamine: Insights from molecular modeling and dynamics simulations. J Phys Chem B 113:15057-15066
23. Hudson L, Liu J, Nath A, Jones M, Raghavan R, Narayan O, Male D, Everall I (2000) Detection of the human immunodeficiency virus regulatory protein tat in CNS tissues. J Neurovirol 6:145-155
24. Kumar AM, Ownby RL, Waldrop-Valverde D, Fernandez B, Kumar M (2011) Human immunodeficiency virus infection in the CNS and decreased dopamine availability: Relationship with neuropsychological performance. J Neurovirol 17:26-40
25. Kumar AM, Fernandez JB, Singer EJ, Commins D, Waldrop-Valverde D, Ownby RL, Kumar M (2009) Human immunodeficiency virus type 1 in the central nervous system leads to decreased dopamine in different regions of postmortem human brains. J Neurovirol 15:257-274
26. Lamers SL, Salemi M, Galligan DC, Morris A, Gray R, Fogel G, Zhao L, McGrath MS (2010) Human immunodeficiency virus-1 evolutionary patterns associated with pathogenic processes in the brain. J Neurovirol 16:230-241
27. Li W, Li G, Steiner J, Nath A (2009) Role of Tat protein in HIV neuropathogenesis. Neurotox Res 16:205-220
28. Li W, Huang Y, Reid R, Steiner J, Malpica-Llanos T, Darden TA, Shankar SK, Mahadevan A, Satishchandra P, Nath A (2008) NMDA receptor activation by HIV-Tat protein is clade dependent. J Neurosci 28:12190-12198
29. Loland CJ, Norgaard-Nielsen K, Gether U (2003) Probing dopamine transporter structure and function by Zn2 + -site engineering. Eur J Pharmacol 479:187-197
30. Loland CJ, Norregaard L, Litman T, Gether U (2002) Generation of an activating Zn(2+) switch in the dopamine transporter: Mutation of an intracellular tyrosine constitutively alters the conformational equilibrium of the transport cycle. Proc Natl Acad Sci U S A 99:1683-1688
31. McArthur JC, Steiner J, Sacktor N, Nath A (2010) Human immunodeficiency virus-associated neurocognitive disorders: Mind the gap. Ann Neurol 67:699-714
32. Meade CS, Conn NA, Skalski LM, Safren SA (2011a) Neurocognitive impairment and medication adherence in HIV patients with and without cocaine dependence. J Behav Med 34:128-138
33. Meade CS, Lowen SB, MacLean RR, Key MD, Lukas SE (2011b) fMRI brain activation during a delay discounting task in HIV-positive adults with and without cocaine dependence. Psychiatry Res 192:167-175
34. Midde NM, Gomez AM, Zhu J (2012) HIV-1 Tat protein decreases dopamine transporter cell surface expression and vesicular monoamine transporter-2 function in Rat striatal synaptosomes. J Neuroimmune Pharmacol 7:629-639
35. Moritz AE, Foster JD, Gorentla BK, Mazei-Robison MS, Yang JW, Sitte HH, Blakely RD, Vaughan RA (2013) Phosphorylation of dopamine transporter serine 7 modulates cocaine analog binding. J Biol Chem 288:20-32
36. Nath A, Clements JE (2011) Eradication of HIV from the brain: Reasons for pause. AIDS 25:577-580
37. Nath A, Maragos WF, Avison MJ, Schmitt FA, Berger JR (2001) Acceleration of HIV dementia with methamphetamine and cocaine. J Neurovirol 7:66-71
38. Norregaard L, Frederiksen D, Nielsen EO, Gether U (1998) Delineation of an endogenous zinc-binding site in the human dopamine transporter. EMBO J 17:4266-4273
39. Peloponese JM Jr, Gregoire C, Opi S, Esquieu D, Sturgis J, Lebrun E, Meurs E, Collette Y, Olive D, Aubertin AM, Witvrow M, Pannecouque C, De Clercq E, Bailly C, Lebreton J, Loret EP (2000) 1H-13C Nuclear magnetic resonance assignment and structural characterization of HIV-1 Tat protein. C R Acad Sci III 323:883-894
40. Purohit V, Rapaka R, Shurtleff D (2011) Drugs of abuse, dopamine, and HIV-associated neurocognitive disorders/HIV-associated dementia. Mol Neurobiol 44:102-110
41. Reith ME, Berfield JL, Wang LC, Ferrer JV, Javitch JA (2001) The uptake inhibitors cocaine and benztropine differentially alter the conformation of the human dopamine transporter. J Biol Chem 276:29012-29018
42. Richfield EK (1993) Zinc modulation of drug binding, cocaine affinity states, and dopamine uptake on the dopamine uptake complex. Mol Pharmacol 43:100-108
43. Robertson KR, Smurzynski M, Parsons TD, Wu K, Bosch RJ, Wu J, McArthur JC, Collier AC, Evans SR, Ellis RJ (2007) The prevalence and incidence of neurocognitive impairment in the HAART era. AIDS 21:1915-1921
44. Shan J, Javitch JA, Shi L, Weinstein H (2011) The substrate-driven transition to an inward-facing conformation in the functional mechanism of the dopamine transporter. PLoS One 6:e16350
45. Sulzer D, Sonders MS, Poulsen NW, Galli A (2005) Mechanisms of neurotransmitter release by amphetamines: A review. Prog Neurobiol 75:406-433
46. Torres GE, Amara SG (2007) Glutamate and monoamine transporters: new visions of form and function. Curr Opin Neurobiol 17:304-312
47. Tozzi V, Balestra P, Bellagamba R, Corpolongo A, Salvatori MF, Visco-Comandini U, Vlassi C, Giulianelli M, Galgani S, Antinori A, Narciso P (2007) Persistence of neuropsychologic deficits despite long-term highly active antiretroviral therapy in patients with HIV-related neurocognitive impairment: Prevalence and risk factors. J Acquir Immune Defic Syndr 45:174-182
48. Wang GJ, Chang L, Volkow ND, Telang F, Logan J, Ernst T, Fowler JS (2004) Decreased brain dopaminergic transporters in HIV-associated dementia patients. Brain 127:2452-2458
49. Westendorp MO, Frank R, Ochsenbauer C, Stricker K, Dhein J, Walczak H, Debatin KM, Krammer PH (1995) Sensitization of T cells to CD95-mediated apoptosis by HIV-1 Tat and gp120. Nature 375:497-500
50. Xiao H, Neuveut C, Tiffany HL, Benkirane M, Rich EA, Murphy PM, Jeang KT (2000) Selective CXCR4 antagonism by Tat: Implications for in vivo expansion of coreceptor use by HIV-1. Proc Natl Acad Sci U S A 97:11466-11471
51. Zhao Y, Terry D, Shi L, Weinstein H, Blanchard SC, Javitch JA (2010) Single-molecule dynamics of gating in a neurotransmitter transporter homologue. Nature 465:188-193
52. Zhu J, Apparsundaram S, Bardo MT, Dwoskin LP (2005) Environmental enrichment decreases cell surface expression of the dopamine transporter in rat medial prefrontal cortex. J Neurochem 93:1434-1443
53. Zhu J, Mactutus CF, Wallace DR, Booze RM (2009) HIV-1 Tat protein-induced rapid and reversible decrease in [3H]dopamine uptake: Dissociation of [3H]dopamine uptake and [3H]2beta-carbomethoxy-3-beta-(4-fluorophenyl)tropane (WIN 35,428) binding in rat striatal synaptosomes. J Pharmacol Exp Ther 329:1071-1083
54. Zhu J, Ananthan S, Mactutus CF, Booze RM (2011) Recombinant human immunodeficiency virus-1 transactivator of transcription1-86 allosterically modulates dopamine transporter activity. Synapse 65:1251-1254