Hiv-1 tat-mediated calcium dysregulation and neuronal dysfunction in vulnerable brain regions

Current Drug Targets

Volumn 17, Issue 1, 2016, Pages 4-14

  Hu, Xiu Ti ^a  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Cognition; Electrophysiology; Medial prefrontal cortex; NeuroAIDS; Neurotoxicity; Over excitation; Pyramidal neuron

Indexed keywords

CALCIUM CHANNEL; GLUTAMIC ACID; GLYCOPROTEIN GP 120; MEMANTINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NIMODIPINE; TRANSACTIVATOR PROTEIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TUMOR NECROSIS FACTOR ALPHA; VPR PROTEIN; CALCIUM CHANNEL L TYPE; TAT PEPTIDE (1-72), HUMAN IMMUNODEFICIENCY VIRUS 1;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ARTICLE; BASAL GANGLION; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CLINICAL TRIAL (TOPIC); EXCITOTOXICITY; HIPPOCAMPUS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; MESENCEPHALON; NERVE INJURY; NEUROLOGIC DISEASE; NEUROTOXICITY; PREFRONTAL CORTEX; UPREGULATION; BRAIN; CALCIUM SIGNALING; ELECTROPHYSIOLOGY; HIV ASSOCIATED DEMENTIA; METABOLISM; PATHOGENICITY; PHYSIOLOGY; PYRAMIDAL NERVE CELL; VIROLOGY;

AIDS DEMENTIA COMPLEX; BRAIN; CALCIUM CHANNELS, L-TYPE; CALCIUM SIGNALING; ELECTROPHYSIOLOGICAL PHENOMENA; HIV-1; HUMANS; PYRAMIDAL CELLS; RECEPTORS, N-METHYL-D-ASPARTATE; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

EID: 84951925602     PISSN: 13894501     EISSN: 18735592     Source Type: Journal    
DOI: 10.2174/1389450116666150531162212     Document Type: Article

References (117)

1. Antinori A, Arendt G, Becker JT, et al. Updated research nosology for HIV-associated neurocognitive disorders. Neurology 2007; 69(18): 1789-99.
2. McArthur JC, Steiner J, Sacktor N, Nath A. Human immunodeficiency virus-associated neurocognitive disorders: Mind the gap. Ann Neurol 2010; 67(6): 699-714.
3. Ferris MJ, Mactutus CF, Booze RM. 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 2008; 32(5): 883-909.
4. Nath A, Schiess N, Venkatesan A, Rumbaugh J, Sacktor N, McArthur J. Evolution of HIV dementia with HIV infection. Int Rev Psychiatry 2008; 20(1): 25-31.
5. Lyon ME, McCarter R, D'Angelo LJ. Detecting HIV associated neurocognitive disorders in adolescents: what is the best screening tool? J Adolesc Health 2009; 44(2): 133-5.
6. Benton TD. Treatment of Psychiatric disorders in children and adolescents with HIV/AIDS. Current Psychiatry Rep 2010; 12: 104-10.
7. Bagashev A, Sawaya BE. Roles and functions of HIV-1 Tat protein in the CNS: an overview. Virol J 2013; 10: 358.
8. Fiala JC, Spacek J, Harris KM. Dendritic spine pathology: cause or consequence of neurological disorders? Brain Res Brain Res Rev 2002; 39(1): 29-54.
9. Nath A. Human immunodeficiency virus (HIV) proteins in neuropathogenesis of HIV dementia. J Infect Dis 2002; 186(Suppl 2): S193-S198.
10. Sa MJ, Madeira MD, Ruela C, Volk B, Mota-Miranda A, Paula- Barbosa MM. Dendritic changes in the hippocampal formation of AIDS patients: a quantitative Golgi study. Acta Neuropathol 2004; 107(2): 97-110.
11. Kim HJ, Martemyanov KA, Thayer SA. Human immunodeficiency virus protein Tat induces synapse loss via a reversible process that is distinct from cell death. J Neurosci 2008; 28(48): 12604-13.
12. Haughey NJ, Mattson MP. Calcium dysregulation and neuronal apoptosis by the HIV-1 proteins Tat and gp120. J Acquir Immune Defic Syndr 2002; 31 Suppl 2: S55-S61.
13. Mattson MP, Haughey NJ, Nath A. Cell death in HIV dementia. Cell Death Differ 2005; 12 Suppl 1: 893-904.
14. Nath A. Human immunodeficiency virus-associated neurocognitive disorder: pathophysiology in relation to drug addiction. Ann N Y Acad Sci 2010; 1187: 122-8.
15. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. 4 ed. New York: Academic Press; 1998.
16. New DR, Maggirwar SB, Epstein LG, Dewhurst S, Gelbard HA. HIV-1 Tat induces neuronal death via tumor necrosis factor-alpha and activation of non-N-methyl-D-aspartate receptors by a NFkappaB-independent mechanism. J Biol Chem 1998; 273(28): 17852-8.
17. Shi B, Raina J, Lorenzo A, Busciglio J, Gabuzda D. Neuronal apoptosis induced by HIV-1 Tat protein and TNF-alpha: potentiation of neurotoxicity mediated by oxidative stress and implications for HIV-1 dementia. J Neurovirol 1998; 4(3): 281-90.
18. McManus CM, Weidenheim K, Woodman SE, et al. Chemokine and chemokine-receptor expression in human glial elements: induction by the HIV protein, Tat, and chemokine autoregulation. Am J Pathol 2000; 156(4): 1441-53.
19. van de Bovenkamp M, Nottet HS, Pereira CF. Interactions of human immunodeficiency virus-1 proteins with neurons: possible role in the development of human immunodeficiency virus-1-associated dementia. Eur J Clin Invest 2002; 32(8): 619-27.
20. Nath A, Anderson C, Jones M, et al. Neurotoxicity and dysfunction of dopaminergic systems associated with AIDS dementia. J Psychopharmacol 2000; 14(3): 222-7.
21. Nath A, Haughey N, Jones M, Anderson C, Bell J, Geiger J. Synergistic neurotoxicity by human immunodeficiency virus proteins Tat and gp120: protection by memantine. Ann Neurol 2000; 47: 186-94.
22. Liu Y, Jones M, Hingtgen CM, et al. 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 2000; 6(12): 1380-7.
23. Chauhan A, Turchan J, Pocernich C, et al. Intracellular human immunodeficiency virus Tat expression in astrocytes promotes astrocyte survival but induces potent neurotoxicity at distant sites via axonal transport. J Biol Chem 2003; 278(15): 13512-9.
24. Lipton SA. AIDS-related dementia and calcium homeostasis. Ann N Y Acad Sci 1994; 747: 205-24.
25. Gonzalez-Scarano F, Martin-Garcia J. The neuropathogenesis of AIDS. Nat Rev Immunol 2005; 5(1): 69-81.
26. King JE, Eugenin EA, Buckner CM, Berman JW. HIV tat and neurotoxicity. Microbes Infect 2006; 8(5): 1347-57.
27. Nath A, Psooy K, Martin C, et al. Identification of a human immunodeficiency virus type 1 Tat epitope that is neuroexcitatory and neurotoxic. J Virol 1996; 70(3): 1475-80.
28. Cheng J, Nath A, Knudsen B, et al. Neuronal excitatory properties of human immunodeficiency virus type 1 Tat protein. Neuroscience 1998; 82(1): 97-106.
29. Bansal AK, Mactutus CF, Nath A, Maragos W, Hauser KF, Booze RM. Neurotoxicity of HIV-1 proteins gp120 and Tat in the rat striatum. Brain Res 2000; 879(1-2): 42-9.
30. Aksenov MY, Hasselrot U, Bansal AK, et al. Oxidative damage induced by the injection of HIV-1 Tat protein in the rat striatum. Neurosci Lett 2001; 305(1): 5-8.
31. Haughey NJ, Nath A, Mattson MP, Slevin JT, Geiger JD. HIV-1 Tat through phosphorylation of NMDA receptors potentiates glutamate excitotoxicity. J Neurochem 2001; 78(3): 457-67.
32. Self RL, Mulholland PJ, Nath A, Harris BR, Prendergast MA. The human immunodeficiency virus type-1 transcription factor Tat produces elevations in intracellular Ca2+ that require function of an N-methyl-D-aspartate receptor polyamine-sensitive site. Brain Res 2003; 995: 39-45.
33. Rom I, Deshmane SL, Mukerjee R, Khalili K, Amini S, Sawaya BE. HIV-1 Vpr deregulates calcium secretion in neural cells. Brain Res 2009; 1275: 81-6.
34. Hegg CC, Hu S, Peterson PK, Thayer SA. Beta-chemokines and human immunodeficiency virus type-1 proteins evoke intracellular calcium increases in human microglia. Neuroscience 2000; 98(1): 191-9.
35. Mayne M, Holden CP, Nath A, Geiger JD. Release of calcium from inositol 1,4,5-trisphosphate receptor-regulated stores by HIV-1 Tat regulates TNF-alpha production in human macrophages. J Immunol 2000; 164(12): 6538-42.
36. Contreras X, Bennasser Y, Chazal N, et al. 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 2005; 332(1): 316-28.
37. Minghetti L, Visentin S, Patrizio M, Franchini L, jmone-Cat MA, Levi G. Multiple actions of the human immunodeficiency virus type-1 Tat protein on microglial cell functions. Neurochem Res 2004; 29(5): 965-78.
38. El-Hage N, Gurwell JA, Singh IN, Knapp PE, Nath A, Hauser KF. Synergistic increases in intracellular Ca2+, and the release of MCP-1, RANTES, and IL-6 by astrocytes treated with opiates and HIV-1 Tat. Glia 2005; 50(2): 91-106.
39. Poggi A, Rubartelli A, Zocchi MR. Involvement of dihydropyridine-sensitive calcium channels in human dendritic cell function. Competition by HIV-1 Tat. J Biol Chem 1998; 273(13): 7205-9.
40. Zocchi MR, Rubartelli A, Morgavi P, Poggi A. HIV-1 Tat inhibits human natural killer cell function by blocking L-type calcium channels. J Immunol 1998; 161(6): 2938-43.
41. Brailoiu GC, Brailoiu E, Chang JK, Dun NJ. Excitatory effects of human immunodeficiency virus 1 Tat on cultured rat cerebral cortical neurons. Neuroscience 2008; 151(3): 701-10.
42. Musante V, Summa M, Neri E, et al. The HIV-1 viral protein Tat increases glutamate and decreases GABA exocytosis from human and mouse neocortical nerve endings. Cereb Cortex 2010; 20(8): 1974-84.
43. Feligioni M, Raiteri L, Pattarini R, et al. The human immunodeficiency virus-1 protein Tat and its discrete fragments evoke selective release of acetylcholine from human and rat cerebrocortical terminals through species-specific mechanisms. J Neurosci 2003; 23(17): 6810-8.
44. Zhu J, Mactutus CF, Wallace DR, Booze RM. HIV-1 Tat proteininduced rapid and reversible decrease in [3H]dopamine uptake: dissociation of [3H]dopamine uptake and [3H]2betacarbomethoxy-3-beta-(4-fluorophenyl)tropane (WIN 35,428) binding in rat striatal synaptosomes. J Pharmacol Exp Ther 2009; 329(3): 1071-83.
45. Ferris MJ, Frederick-Duus D, Fadel J, Mactutus CF, Booze RM. Hyperdopaminergic tone in HIV-1 protein treated rats and cocaine sensitization. J Neurochem 2010; 115(4): 885-96.
46. Wang GJ, Chang L, Volkow ND, et al. Decreased brain dopaminergic transporters in HIV-associated dementia patients. Brain 2004; 127(Pt 11): 2452-8.
47. Chang L, Wang GJ, Volkow ND, et al. Decreased brain dopamine transporters are related to cognitive deficits in HIV patients with or without cocaine abuse. Neuroimage 2008; 42(2): 869-78.
48. Aksenova MV, Silvers JM, Aksenov MY, et al. HIV-1 Tat neurotoxicity in primary cultures of rat midbrain fetal neurons: changes in dopamine transporter binding and immunoreactivity. Neurosci Lett 2006; 395(3): 235-9.
49. Haughey NJ, Holden CP, Nath A, Geiger JD. Involvement of inositol 1,4,5-trisphosphate-regulated stores of intracellular calcium in calcium dysregulation and neuron cell death caused by HIV-1 protein tat. J Neurochem 1999; 73(4): 1363-74.
50. Prendergast MA, Rogers DT, Mulholland PJ, et al. Neurotoxic effects of the human immunodeficiency virus type-1 transcription factor Tat require function of a polyamine sensitive-site on the Nmethyl-D-aspartate receptor. Brain Res 2002; 954(2): 300-7.
51. Chandra T, Maier W, Konig HG, et al. Molecular interactions of the type 1 human immunodeficiency virus transregulatory protein Tat with N-methyl-d-aspartate receptor subunits. Neuroscience 2005; 134(1): 145-53.
52. Norman JP, Perry SW, Kasischke KA, Volsky DJ, Gelbard HA. HIV-1 trans activator of transcription protein elicits mitochondrial hyperpolarization and respiratory deficit, with dysregulation of complex IV and nicotinamide adenine dinucleotide homeostasis in cortical neurons. J Immunol 2007; 178(2): 869-76.
53. Norman JP, Perry SW, Reynolds HM, et al. HIV-1 Tat activates neuronal ryanodine receptors with rapid induction of the unfolded protein response and mitochondrial hyperpolarization. PLoS ONE 2008; 3(11): e3731.
54. Perry SW, Barbieri J, Tong N, et al. Human immunodeficiency virus-1 Tat activates calpain proteases via the ryanodine receptor to enhance surface dopamine transporter levels and increase transporter-specific uptake and Vmax. J Neurosci 2010; 30(42): 14153-64.
55. Hamilton NB, Attwell D. Do astrocytes really exocytose neurotransmitters? Nat Rev Neurosci 2010; 11(4): 227-38.
56. Eugenin EA, D'Aversa TG, Lopez L, Calderon TM, Berman JW. MCP-1 (CCL2) protects human neurons and astrocytes from NMDA or HIV-tat-induced apoptosis. J Neurochem 2003; 85(5): 1299-311.
57. Eugenin EA, King JE, Hazleton JE, et al. Differences in NMDA receptor expression during human development determine the response of neurons to HIV-tat-mediated neurotoxicity. Neurotox Res 2011; 19(1): 138-48.
58. Jara JH, Singh BB, Floden AM, Combs CK. Tumor necrosis factor alpha stimulates NMDA receptor activity in mouse cortical neurons resulting in ERK-dependent death. J Neurochem 2007; 100(5): 1407-20.
59. Ye L, Huang Y, Zhao L, et al. IL-1beta and TNF-alpha induce neurotoxicity through glutamate production: a potential role for neuronal glutaminase. J Neurochem 2013; 125(6): 897-908.
60. Zhou BY, Liu Y, Kim B, Xiao Y, He JJ. Astrocyte activation and dysfunction and neuron death by HIV-1 Tat expression in astrocytes. Mol Cell Neurosci 2004; 27(3): 296-305.
61. Eugenin EA, King JE, Nath A, et al. HIV-tat induces formation of an LRP-PSD-95- NMDAR-nNOS complex that promotes apoptosis in neurons and astrocytes. Proc Natl Acad Sci USA 2007 Feb 27; 104(9): 3438-43.
62. Eugenin EA, Berman JW. Gap junctions mediate human immunodeficiency virus-bystander killing in astrocytes. J Neurosci 2007; 27(47): 12844-50.
63. Krogh KA, Lyddon E, Thayer SA. HIV-1 Tat activates a RhoA signaling pathway to reduce NMDA-evoked calcium responses in hippocampal neurons via an actin-dependent mechanism. J Neurochem 2015; 132(3): 354-66.
64. Krogh KA, Lyddon E, Thayer SA. HIV-1 Tat activates a RhoA signaling pathway to reduce NMDA-evoked calcium responses in hippocampal neurons via an actin-dependent mechanism. J Neurochem 2014 Aug 25.
65. Wheeler D, Knapp E, Bandaru VV, et al. Tumor necrosis factoralpha-induced neutral sphingomyelinase-2 modulates synaptic plasticity by controlling the membrane insertion of NMDA receptors. J Neurochem 2009; 109(5): 1237-49.
66. Rostasy K, Monti L, Lipton SA, Hedreen JC, Gonzalez RG, Navia BA. HIV leucoencephalopathy and TNFalpha expression in neurones. J Neurol Neurosurg Psychiatry 2005; 76(7): 960-4.
67. Tseng KY, O'Donnell P. Dopamine-glutamate interactions controlling prefrontal cortical pyramidal cell excitability involve multiple signaling mechanisms. J Neurosci 2004; 24(22): 5131-9.
68. Tseng KY, O'Donnell P. Post-pubertal emergence of prefrontal cortical up states induced by D1-NMDA co-activation. Cereb Cortex 2005; 15(1): 49-57.
69. Chen BS, Roche KW. Regulation of NMDA receptors by phosphorylation. Neuropharmacology 2007; 53(3): 362-8.
70. Zidovetzki R, Wang JL, Chen P, Jeyaseelan R, Hofman F. Human immunodeficiency virus Tat protein induces interleukin 6 mRNA expression in human brain endothelial cells via protein kinase Cand cAMP-dependent protein kinase pathways. AIDS Res Hum Retroviruses 1998; 14(10): 825-33.
71. Hofmann B, Nishanian P, Nguyen T, Insixiengmay P, Fahey JL. Human immunodeficiency virus proteins induce the inhibitory cAMP/protein kinase A pathway in normal lymphocytes. Proc Natl Acad Sci USA 1993; 90(14): 6676-80.
72. Hofmann B, Nishanian P, Nguyen T, Liu M, Fahey JL. Restoration of T-cell function in HIV infection by reduction of intracellular cAMP levels with adenosine analogues. AIDS 1993; 7(5): 659-64.
73. Liu X, Chang L, Vigorito M, Kass M, Li H, Chang SL. Methamphetamine-induced behavioral sensitization is enhanced in the HIV-1 transgenic rat. J Neuroimmune Pharmacol 2009; 4(3): 309-16.
74. Silvers JM, Aksenova MV, Aksenov MY, Mactutus CF, Booze RM. Neurotoxicity of HIV-1 Tat protein: involvement of D1 dopamine receptor. Neurotoxicology 2007; 28(6): 1184-90.
75. Aksenov MY, Aksenova MV, Mactutus CF, Booze RM. D1/NMDA receptors and concurrent methamphetamine+ HIV-1 Tat neurotoxicity. J Neuroimmune Pharmacol 2012; 7(3): 599-608.
76. Goretzki L, Mueller BM. Low-density-lipoprotein-receptor-related protein (LRP) interacts with a GTP-binding protein. Biochem J 1998; 336 (Pt 2): 381-6.
77. Ekokoski E, Aitio O, Tornquist K, Yli-Kauhaluoma J, Tuominen RK. HIV-1 Tat-peptide inhibits protein kinase C and protein kinase A through substrate competition. Eur J Pharm Sci 2010; 40(5): 404-11.
78. Maggirwar SB, Tong N, Ramirez S, Gelbard HA, Dewhurst S. HIV-1 Tat-mediated activation of glycogen synthase kinase-3beta contributes to Tat-mediated neurotoxicity. J Neurochem 1999; 73(2): 578-86.
79. Sharma A, Hu XT, Napier TC, Al-Harthi L. Methamphetamine and HIV-1 Tat down regulate beta-catenin signaling: implications for methampetamine abuse and HIV-1 co-morbidity. J Neuroimmune Pharmacol 2011; 6(4): 597-607.
80. Henderson L, Sharma A, Monaco MCG, Major EO, Al-Harthi L. Human immunodeficiency virus type 1 (HIV-1) Tansactivator of transcription through its intact core and cysteine-rich domains inhibits Wnt/beta-catenin signaling in astrocytes: relevance to HIV neuropathogenesis. J Neuroscie 2012; 32(46): 16306-13.
81. Al-Harthi L. Interplay between Wnt/beta-catenin signaling and HIV: virologic and biologic consequences in the CNS. J Neuroimmune Pharmacol 2012; 7(4): 731-9.
82. Al-Harthi L. Wnt/beta-catenin and its diverse physiological cell signaling pathways in neurodegenerative and neuropsychiatric disorders. J Neuroimmune Pharmacol 2012; 7(4): 725-30.
83. Strijbos PJ, Zamani MR, Rothwell NJ, Arbuthnott G, Harkiss G. Neurotoxic mechanisms of transactivating protein Tat of Maedi-Visna virus. Neurosci Lett 1995; 197(3): 215-8.
84. Albini A, Ferrini S, Benelli R, et al. HIV-1 Tat protein mimicry of chemokines. Proc Natl Acad Sci USA 1998; 95(22): 13153-8.
85. Wayman WN, Dodiya HB, Persons AL, et al. Enduring cortical alterations after a single in vivo treatment of HIV-1 Tat. Neuroreport 2012; 23: 825-9.
86. Wayman W, Chen L, Napier TC, Hu X-T. Cocaine selfadministration enhances excitatory responses of pyramidal neurons in the rat medial prefrontal cortex to HIV-1 Tat. Eur J Neurosci 2015; 41(9): 1195-1206.
87. Napier TC, Chen L, Kashanchi F, Hu X-T. Repeated cocaine treatment enhances HIV-1 Tat-induced cortical excitability via over-activation of L-type calcium channels. J Neuroimmune Pharmacol 2014; 9(3): 354-368.
88. Green EM, Barrett CF, Bultynck G, Shamah SM, Dolmetsch RE. The tumor suppressor eIF3e mediates calcium-dependent internalization of the L-type calcium channel CaV1.2. Neuron 2007; 55(4): 615-32.
89. Reid W, Sadowska M, Denaro F, et al. An HIV-1 transgenic rat that develops HIV-related pathology and immunologic dysfunction. Proc Natl Acad Sci USA 2001; 98(16): 9271-6.
90. Liao P, Yu D, Lu S, et al. Smooth muscle-selective alternatively spliced exon generates functional variation in Cav1.2 calcium channels. J Biol Chem 2004; 279(48): 50329-35.
91. Graf EM, Bock M, Heubach JF, et al. Tissue distribution of a human Ca v 1.2 alpha1 subunit splice variant with a 75 bp insertion. Cell Calcium 2005; 38(1): 11-21.
92. Biel M, Ruth P, Bosse E, et al. Primary structure and functional expression of a high voltage activated calcium channel from rabbit lung. FEBS Lett 1990; 269(2): 409-12.
93. Catterall WA. Voltage-gated calcium channels. Cold Spring Harb Perspect Biol 2011; 3(8): 1-23.
94. Yasuda T, Chen L, Barr W, et al. Auxiliary subunit regulation of high-voltage activated calcium channels expressed in mammalian cells. Eur J Neurosci 2004; 20(1): 1-13.
95. Yasuda T, Lewis RJ, Adams DJ. Overexpressed Ca(v)beta3 inhibits N-type (Cav2.2) calcium channel currents through a hyperpolarizing shift of ultra-slow and closed-state inactivation. J Gen Physiol 2004; 123(4): 401-16.
96. Furukawa K, Mattson MP. The transcription factor NF-kappaB mediates increases in calcium currents and decreases in NMDA and AMPA/kainate-induced currrents induced by tumor necrosis factor-alpha in hippocampal neurons. J Neurochem 1998; 70(5): 1876-86.
97. Pollock J, McFarlane SM, Connell MC, et al. TNF-alpha receptors simultaneously activate Ca2+ mobilisation and stress kinases in cultured sensory neurones. Neuropharmacology 2002; 42(1): 93-106.
98. Ford KA, Wolf ME, Hu XT. Plasticity of L-type Ca2+ channels after cocaine withdrawal. Synapse 2009; 63(8): 690-7.
99. Heng L, Markham JA, Hu XT, Tseng KY. Concurrent upregulation of postynaptic L-type Ca2+ channel function and protein kinase A signaling is required for the periadolescent facilitation of Ca2+ plateau potentials in the prefrontal cortex. Neuropharmacology 2011; 60(6): 953-62.
100. Markram H, Sakmann B. Calcium transients in dendrites of neocortical neurons evoked by single subthreshold excitatory postsynaptic potentials via low-voltage-activated calcium channels. Proc Natl Acad Sci USA 1994; 91(11): 5207-11.
101. Markram H, Lubke J, Frotscher M, Sakmann B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 1997; 275: 213-5.
102. Wang Z, Kai L, Day M, et al. Dopaminergic control of corticostriatal long-term synaptic depression in medium spiny neurons is mediated by cholinergic interneurons. Neuron 2006; 50(3): 443-52.
103. Lipscombe D. L-type calcium channels - Highs and new lows. Circ Res 2002; 90(9): 933-5.
104. Kruman II, Nath A, Mattson MP. HIV-1 protein Tat induces apoptosis of hippocampal neurons by a mechanism involving caspase activation, calcium overload, and oxidative stress. Exp Neurol 1998; 154(2): 276-88.
105. Abramowitz J, Birnbaumer L. Physiology and pathophysiology of canonical transient receptor potential channels. FASEB J 2009; 23(2): 297-328.
106. Birnbaumer L. The TRPC class of ion channels: a critical review of their roles in slow, sustained increases in intracellular Ca(2+) concentrations. Annu Rev Pharmacol Toxicol 2009; 49: 395-426.
107. Zholos AV. TRPC5. Handb Exp Pharmacol 2014; 222: 129-56.
108. Bollimuntha S, Singh BB, Shavali S, Sharma SK, Ebadi M. TRPC1-mediated inhibition of 1-methyl-4-phenylpyridinium ion neurotoxicity in human SH-SY5Y neuroblastoma cells. J Biol Chem 2005; 280(3): 2132-40.
109. Bollimuntha S, Ebadi M, Singh BB. TRPC1 protects human SHSY5Y cells against salsolinol-induced cytotoxicity by inhibiting apoptosis. Brain Res 2006; 1099(1): 141-9.
110. Jia Y, Zhou J, Tai Y, Wang Y. TRPC channels promote cerebellar granule neuron survival. Nat Neurosci 2007; 10(5): 559-67.
111. Yao H, Peng F, Dhillon N, et al. Involvement of TRPC channels in CCL2-mediated neuroprotection against tat toxicity. J Neurosci 2009; 29(6): 1657-69.
112. Satoh S, Tanaka H, Ueda Y, et al. Transient receptor potential (TRP) protein 7 acts as a G protein-activated Ca2+ channel mediating angiotensin II-induced myocardial apoptosis. Mol Cell Biochem 2007; 294(1-2): 205-15.
113. Foller M, Kasinathan RS, Duranton C, Wieder T, Huber SM, Lang F. PGE2-induced apoptotic cell death in K562 human leukaemia cells. Cell Physiol Biochem 2006; 17(5-6): 201-10.
114. Yao H, Peng F, Fan Y, Zhu X, Hu G, Buch SJ. TRPC channelmediated neuroprotection by PDGF involves Pyk2/ERK/CREB pathway. Cell Death Differ 2009; 16(12): 1681-93.
115. Peng F, Yao H, Akturk HK, Buch S. Platelet-derived growth factor CC-mediated neuroprotection against HIV Tat involves TRPCmediated inactivation of GSK 3beta. PLoS ONE 2012; 7(10): e47572.
116. Schifitto G, Navia BA, Yiannoutsos CT, et al. Memantine and HIV-associated cognitive impairment: a neuropsychological and proton magnetic resonance spectroscopy study. AIDS 2007; 21(14): 1877-86.
117. Navia BA, Dafni U, Simpson D, et al. A phase I/II trial of nimodipine for HIV-related neurologic complications. Neurology 1998; 51(1): 221-228.