Repeated cocaine treatment enhances HIV-1 Tat-induced cortical excitability via over-activation of L-type calcium channels

Journal of Neuroimmune Pharmacology

Volumn 9, Issue 3, 2014, Pages 354-368

  Napier, T Celeste ^a   Chen, Lihua ^a   Kashanchi, Fatah ^b   Hu, Xiu Ti ^a  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

^b GEORGE MASON UNIVERSITY   (United States)

Author keywords

HIV 1 protein; Medial prefrontal cortex; NeuroAIDS; Neuropathophysiology; Neurotoxicity; Pyramidal neuron

Indexed keywords

CALCIUM CHANNEL L TYPE; CALCIUM ION; COCAINE; DILTIAZEM; SODIUM CHLORIDE; TRANSACTIVATOR PROTEIN;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIUM TRANSPORT; ELECTROPHYSIOLOGY; FOREBRAIN; HUMAN IMMUNODEFICIENCY VIRUS 1; LONG TERM EXPOSURE; MALE; MEMBRANE DEPOLARIZATION; NERVE CELL EXCITABILITY; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; ACTION POTENTIAL; ANIMAL; BRAIN CORTEX; DRUG EFFECTS; METABOLISM; NERVE CELL; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; SPRAGUE DAWLEY RAT; TOXICITY;

ACTION POTENTIALS; ANIMALS; CALCIUM CHANNELS, L-TYPE; CEREBRAL CORTEX; COCAINE; MALE; NEURONS; ORGAN CULTURE TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

EID: 84901255154     PISSN: 15571890     EISSN: 15571904     Source Type: Journal    
DOI: 10.1007/s11481-014-9524-6     Document Type: Article

References (57)

1. Allen TGJ, Sim JA, Brown DA (1993) The whole-cell calcium current in acutely dissociated magnocellular cholinergic basal forebrain neurones of the rat. J Physiol Lond 460:91-116 (Pubitemid 23058040)
2. Antinori A et al (2007) Updated research nosology for HIV-associated neurocognitive disorders. Neurology 69:1789-1799 (Pubitemid 350059308)
3. Avraham HK, Jiang S, Lee TH, Prakash O, Avraham S (2004) HIV-1 Tat-mediated effects on focal adhesion assembly and permeability in brain microvascular endothelial cells. J Immunol 173:6228-6233 (Pubitemid 39487780)
4. Bonavia R, Bajetto A, Barbero S, Albini A, Noonan DM, Schettini G (2001) HIV-1 Tat causes apoptotic death and calcium homeostasis alterations in rat neurons. BiochemBiophys Res Commun 288:301-308 (Pubitemid 33022484)
5. Brailoiu GC, Brailoiu E, Chang JK, Dun NJ (2008) Excitatory effects of human immunodeficiency virus 1 Tat on cultured rat cerebral cortical neurons. Neuroscience 151:701-710
6. Campbell GR, Loret EP (2009) What does the structure-function relationship of the HIV-1 Tat protein teach us about developing anAIDS vaccine? Retrovirology 6:50
7. Catterall WA, Striessnig J, Snutch TP, Perez-Reyes E (2003) International Union of Pharmacology. XL. Compendium of voltage-gated ion channels: calcium channels. Pharmacol Rev 55:579-581 (Pubitemid 37500517)
8. Cheng J, Nath A, Knudsen B, Hochman S, Geiger JD, Ma M, Magnuson DS (1998) Neuronal excitatory properties of human immunodeficiency virus type 1 Tat protein. Neuroscience 82:97-106
9. Cohn SE, Jiang H, McCutchan JA, Koletar SL et al (2011) Association of ongoing drug and alcohol use with non-adherence to aniretroviral therapy and higher risk of AIDS and death: results from ACTG 362. AIDS Care 23:775-785
10. Contreras X, Bennasser Y, Chazal N, Moreau M, Leclerc C, Tkaczuk J, Bahraoui E (2005) Human immunodeficiency virus type 1 Tat protein induces an intracellular calcium increase in human monocytes that requires DHP receptors: involvement in TNF-alpha production. Virology 332:316-328
11. Dolmetsch RE, Pajvani U, Fife K, Spotts JM, Greenberg ME (2001) Signaling to the nucleus by an L-type calcium channel-calmodulin complex through the MAP kinase pathway. Science 294:333-339 (Pubitemid 32963394)
12. Eugenin EA, King JE, Nath A, Calderon TM, Zukin RS, Bennett MV, Berman JW (2007) HIV-tat induces formation of an LRP-PSD-95-NMDAR-nNOS complex that promotes apoptosis in neurons and astrocytes. Proc Natl Acad Sci U S A 104:3438-3443 (Pubitemid 46364177)
13. 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
14. Ford KA, Wolf ME, Hu XT (2009) Plasticity of L-type Ca2+ channels after cocaine withdrawal. Synapse 63:690-697
15. Glossmann H, Linn T, Rombusch M, Ferry DR (1983) Temperature-dependent regulation of d-cis-[3H]diltiazem binding to Ca2+ channels by 1,4-dihydropyridine channel agonists and antagonists. FEBS Lett 160:226-232 (Pubitemid 13048742)
16. Goldstein RZ, Volkow ND (2011) Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications. Nat Rev Neurosci 12:652-669
17. Gorelova N, Yang CR (1997) The course of neural projection from the prefrontal cortex to the nucleus accumbens in the rat. Neuroscience 76:689-706 (Pubitemid 27013410)
18. Griffith WH, Matthews RT (1986) Electrophysiology of AChE-positive neurons in basal forebrain slices. Neurosci Lett 71:169-174 (Pubitemid 17176504)
19. Haughey NJ, Mattson MP (2002) Calcium dysregulation and neuronal apoptosis by the HIV-1 proteins Tat and gp120. J Acquir Immune Defic Syndr 31(Suppl 2):S55-S61 (Pubitemid 35190559)
20. Haughey NJ, Nath A, Mattson MP, Slevin JT, Geiger JD (2001) HIV-1 Tat through phosphorylation of NMDA receptors potentiates glutamate excitotoxicity. J Neurochem 78:457-467 (Pubitemid 32729974)
21. Hayton SJ, Lovett-Barron M, Dumont EC, Olmstead MC (2010) Target-specific encoding of response inhibition: increased contribution of AMPA to NMDA receptors at excitatory synapses in the prefrontal cortex. J Neurosci 30:11493-11500
22. Hu X-T (2007) Cocaine withdrawal and neuro-adaptations in ion channel function. Mol Neurobiol 35:95-112
23. Hu X-T, Basu S, White FJ (2004) Repeated cocaine administration suppresses HVA-Ca2+ potentials and enhances activity of K +channels in rat nucleus accumbens neurons. J Neurophysiol 92:1597-1607 (Pubitemid 39100658)
24. Kalivas PW, Volkow ND (2011) New medications for drug addiction hiding in glutamatergic neuroplasticity. Mol Psychiatry 16:974-986
25. Khateb A, Mühlethaler M, Alonso A, Serafin M, Mainville L, Jones BE (1992) Cholinergic nucleus basalis neurons display the capacity for rhythmic bursting activity mediated by low-threshold calcium spikes. Neuroscience 51:489-494
26. 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
27. Li W, Li G, Steiner J, Nath A (2009) Role of Tat protein in HIV neuropathogenesis. Neurotox Res 16:205-220
28. Lipscombe D (2002) L-type calciumchannels - Highs and new lows. Circ Res 90:933-935
29. Liu Y, Jones M, Hingtgen CM, Bu G, Laribee N, Tanzi RE, Moir RD, Nath A, He JJ (2000) Uptake of HIV-1 tat protein mediated by low-density lipoprotein receptor-related protein disrupts the neuronal metabolic balance of the receptor ligands. Nat Med 6: 1380-1387 (Pubitemid 32001023)
30. Markram H, Sakmann B (1994) Calcium transients in dendrites of neocortical neurons evoked by single subthreshold excitatory postsynaptic potentials via low-voltage-activated calcium channels. Proc Natl Acad Sci U S A 91:5207-5211 (Pubitemid 24177822)
31. Markram H, Lubke J, Frotscher M, Sakmann B (1997) Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275:213-215 (Pubitemid 27034762)
32. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5:793-807 (Pubitemid 39336216)
33. Nasif FJ, Hu XT, White FJ (2005a) Repeated cocaine administration increases voltage-sensitive calcium currents in response to membrane depolarization in medial prefrontal cortex pyramidal neurons. J Neurosci 25:3674-3679
34. Nasif FJ, Sidiropoulou K, Hu XT, White FJ (2005b) Repeated cocaine administration increases membrane excitability of pyramidal neurons in the rat medial prefrontal cortex. J Pharmacol Exp Ther 312:1305-1313 (Pubitemid 40293794)
35. Nath A (2010) Human immunodeficiency virus-associated neurocognitive disorder: pathophysiology in relation to drug addiction. Ann N YAcad Sci 1187:122-128
36. Nath A, Psooy K, Martin C, Knudsen B, Magnuson DS, Haughey N, Geiger JD (1996) Identification of a human immunodeficiency virus type 1 Tat epitope that is neuroexcitatory and neurotoxic. J Virol 70: 1475-1480 (Pubitemid 26062905)
37. Nath A, Conant K, Chen P, Scott C, Major EO (1999) Transient exposure to HIV-1 Tat protein results in cytokine production in macrophages and astrocytes.A hit and run phenomenon. J Biol Chem 274:17098-17102
38. Nath A, Haughey NJ, Jones M, Anderson C, Bell JE, Geiger JD (2000) Synergistic neurotoxicity by human immunodeficiency virus proteins Tat and gp120: protection by memantine. Ann Neurol 47:186-194 (Pubitemid 30078565)
39. Niimi Y, Hino N, Ochi R (2003) Diltiazem facilitates inactivation of single L-type calcium channels in guinea pig ventricular myocytes. Jpn Heart J 44:1005-1014 (Pubitemid 41518955)
40. Paris JJ, Carey AN, Shay CF, Gomes SM, He JJ, McLaughlin JP (2014) Effects of Conditional Central Expression of HIV-1 Tat Protein to Potentiate Cocaine-Mediated Psychostimulation and Reward Among Male Mice. Neuropsychopharmacology 39:380-388
41. Paxinos G, Watson C (1998) The Rat Brain in Stereotaxic Coordinates. Academic Press, New York
42. Perez MF, Ford KA, Goussakov I, Stutzmann GE, Hu XT (2011) Repeated cocaine exposure decreases dopamine D2-like receptor modulation of Ca(2+) homeostasis in rat nucleus accumbens neurons. Synapse 65:168-180
43. Pocernich CB, Sultana R, Mohmmad-Abdul H, Nath A, Butterfield DA (2005) HIV-dementia, Tat-induced oxidative stress, and antioxidant therapeutic considerations. Brain Res Brain Res Rev 50:14-26 (Pubitemid 41607513)
44. Price TO, Ercal N, Nakaoke R, Banks WA (2005) HIV-1 viral proteins gp120 and Tat induce oxidative stress in brain endothelial cells. Brain Res 1045:57-63 (Pubitemid 40725220)
45. Rumbaugh JA, Li G, Rothstein J, Nath A (2007) Ceftriaxone protects against the neurotoxicity of human immunodeficiency virus proteins. J Neurovirol 13:168-172 (Pubitemid 46780092)
46. Stuber GD, Hopf FW, Tye KM, Chen BT, Bonci A (2010) Neuroplastic alterations in the limbic system following cocaine or alcohol exposure. Curr Top Behav Neurosci 3:3-27
47. The National Research Council (1996) Guide for the Care and Use of Laboratory Animals (NIH Publication N. 85-23).
48. Tiwari S, Nair MP, Saxena SK (2013) Latest trends in drugs of abuse - HIV infection and neuroAIDS. Future Virol 8:121-127
49. Verdejo-Garcia A, Bechara A, Recknor EC, Perez-Garcia M (2006) Executive dysfunction in substance dependent individuals during drug use and abstinence: An examination of the behavioral, cognitive and emotional correlates of addiction. J Int Neuropsychol Soc 12:405-415 (Pubitemid 43970906)
50. Volkow ND, Wang GJ, Ma Y, Fowler JS et al (2005) Activation of orbital and medial prefrontal cortex by methylphenidate in cocaineaddicted subjects but not in controls: relevance to addiction. J Neurosci 25:3932-3939 (Pubitemid 40570426)
51. Wayman WN, Dodiya HB, Persons AL, Kashanchi F, Kordower JH, Hu X-T, Napier TC (2012) Enduring cortical alterations after a single in vivo treatment of HIV-1 Tat. Neuroreport 23:825-829
52. 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
53. Wolf ME (1998) The role of excitatory amino acids in behavioral sensitization to psychomotor stimulants. Prog Neurobiol 54:679-720
54. 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
55. Yuste R (2005) Origin and classification of neocortical interneurons. Neuron 48:524-527
56. Zhang X-F, Hu X-T, White FJ (1998) Whole-cell plasticity in cocaine withdrawal:reduced sodium currents in nucleus accumbens neurons. J Neuroscience 18:488-498 (Pubitemid 28046806)
57. Zocchi MR, Rubartelli A, Morgavi P, Poggi A (1998) HIV-1 Tat inhibits human natural killer cell function by blocking L-type calcium channels. J Immunol 161:2938-2943 (Pubitemid 28425717)