HIV-1 Tat activates neuronal ryanodine receptors with rapid induction of the unfolded protein response and mitochondrial hyperpolarization

PLoS ONE

Volumn 3, Issue 11, 2008, Pages

  Norman, John P ^a   Perry, Seth W ^a   Reynolds, Holly M ^a   Kiebala, Michelle ^a   De Mesy Bentley, Karen L ^a   Trejo, Margarita ^c   Volsky, David J ^b   Maggirwar, Sanjay B ^a   Dewhurst, Stephen ^a   Masliah, Eliezer ^c   Gelbard, Harris A ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; RYANODINE RECEPTOR; TRANSACTIVATOR PROTEIN;

ANIMAL CELL; ARTICLE; BRAIN CELL; CALCIUM CELL LEVEL; CELL STRUCTURE; CENTRAL NERVOUS SYSTEM INFECTION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENERGY METABOLISM; ENZYME ACTIVATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HYPERPOLARIZATION; IN VITRO STUDY; INFLAMMATION; MALE; MITOCHONDRION; MOUSE; NERVE DEGENERATION; NEUROPATHOLOGY; NONHUMAN; PROTEIN FUNCTION; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; ACQUIRED IMMUNE DEFICIENCY SYNDROME; ANIMAL; BRAIN CORTEX; C57BL MOUSE; CHANNEL GATING; CYTOLOGY; DRUG EFFECT; METABOLISM; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL MEMBRANE POTENTIAL; NERVE CELL; PATHOLOGY; PROTEIN FOLDING; PROTEIN TRANSPORT; RAT; SPRAGUE DAWLEY RAT; ULTRASTRUCTURE; UPREGULATION;

HUMAN IMMUNODEFICIENCY VIRUS 1; MURINAE;

AIDS DEMENTIA COMPLEX; ANIMALS; CALCIUM; CEREBRAL CORTEX; ENDOPLASMIC RETICULUM; HUMANS; ION CHANNEL GATING; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; NEURONS; PROTEIN FOLDING; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; UP-REGULATION;

EID: 56649102055     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0003731     Document Type: Article

References (66)

1. Davis LE, Hjelle BL, Miller VE, Palmer DL, Llewellyn AL, et al. (1992) Early viral brain invasion in iatrogenic human immunodeficiency virus infection. Neurology 42: 1736-1739.
2. Ellis RO, Langford D, Masliah E (2007) HIV and antiretroviral therapy in the brain: neuronal injury and repair. Nature Rev Neurosci 8: 33-45.
3. Robertson KR, Smurzynski M, Parsons TD, Wu K, Bosch RJ, et al. (2007) The prevalence and incidence of neurocognitive impairment in the HAART era. AIDS 21(14): 1915-1921.
4. Kerza-Kwiatecki AP, Amini S (1999) CNS as an HIV-1 reservoir; BBB and drug delivery. J Neurovirol 5: 113-114.
5. McArthur JC (2004) HIV dementia: an evolving disease. J Neuroimmunol 157: 3-10.
6. van de Bovenkamp M, Nottet HS, Pereira CF (2002) 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 32: 619-627.
7. Ozdener H (2005) Molecular mechanisms of HIV-1 associated neurodegeneration. J Biosci 30: 391-405.
8. Porcheray F, Leone C, Samah B, Rimaniol AC, Dereuddre-Bosquet N, et al. (2006) Glutamate metabolism in HIV-infected macrophages: implications for the CNS. Am J Physiol Cell Physiol 291: C618-626.
9. Wang Z, Pekarskaya O, Bencheikh M, Chao W, Gelbard HA, et al. (2003) Reduced expression of glutamate transporter EAAT2 and impaired glutamate transport in human primary astrocytes exposed to HIV-1 or gp120. Virology 312: 60-73.
10. Nath A, Geiger J (1998) Neurobiological aspects of human immunodeficiency virus infection: neurotoxic mechanisms. Prog Neurobiol 54: 19-33.
11. Perry SW, Hamilton JA, Tjoelker LW, Dbaibo D, Dzenko KA, et al. (1998) Platelet-activating factor receptor activation. An initiator step in HIV-1 neuropathogenesis. J Biol Chem 273: 17660-17664.
12. Kaul M, Garden GA, Lipton SA (2001) Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature 410: 988-994.
13. Bellizzi MJ, Lu SM, Masliah E, Gelbard HA (2005) Synaptic activity becomes excitotoxic in neurons exposed to elevated levels of platelet-activating factor. J Clin Inv 115(11): 3185-3192.
14. An SF, Giometto B, Groves M, Miller RF, Beckett AA, et al. (1997) Axonal damage revealed by accumulation of beta-APP in HIV-positive individuals without AIDS. J Neuropathol Exp Neurol 56(11): 1262-1268.
15. Gelbard HA, James H, Sharer L, Perry SW, Saito Y, et al. (1995) Identification of apoptotic neurons in post-mortem brain tissue with HIV-1 encephalitis and progressive encephalopathy. Neuropathol Appl Neurobiol 21: 208-217.
16. Adle-Biassette H, Levy Y, Colombel M, Poron F, Natchev S, et al. (1995) Neuronal apoptosis in HIV infection in adults. Neuropathol Appl Neurobiol 21: 218-227.
17. Gendelman HE, Diesing S, Gelbard HA, Swindells S (2002) The Neuropathogenesis of HIV-1 Infection. In: Wormser, ed. AIDS and Other Manifestations of HIV Infections 4th edition. pp 86-91.
18. Weis S, Haug H, Budka H (1996) Vascular changes in the cerebral cortex in HIV-1 infection: I. A morphometric investigation by light and electron microscopy. Clin Neuropathol 15(6): 361-366.
19. van de Bovenkamp M, Nottet HS, Pereira CF (2002) 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 32: 619-627.
20. Ensoli B, Barillari G, Salahuddin SZ, Gallo RC, Wong-Staal F (1990) Tat protein of HIV-1 stimulates growth of cells derived from Kaposi's sarcoma lesions of AIDS patients. Nature 345: 84-86.
21. Brigati C, Giacca M, Noonan DM, Albini A (2003) HIV Tat, its TARgets and the control of viral gene expression. FEMS Microbiol Lett 220: 57-65.
22. Xiao H, Neuveut C, Tiffany HL, Benkirane M, Rich EA, et al. (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.
23. Frankel AD, Pabo CO (1988) Cellular uptake of the tat protein from human immunodeficiency virus. Cell 55: 1189-1193.
24. Tardieu M, Hery C, Peudenier S, Boespflug O, Montagnier L (1992) Human immunodeficiency virus type 1-infected monocytic cells can destroy human neural cells after cell-to-cell adhesion. Ann Neurol 32: 11-17.
25. Vives E, Brodin P, Lebleu B (1997) A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J Biol Chem 272: 16010-16017.
26. Del Gaizo V, MacKenzie JA, Payne RM (2003) Targeting proteins to mitochondria using TAT. Mol Genet Metab 80: 170-180.
27. Haughey NJ, Holden CP, Nath A, Geiger JD (1999) 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 73: 1363-1374.
28. 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.
29. Murakami T, Hino SI, Saito A, Imaizumi K (2007) Endoplasmic reticulum stress response in dendrites of cultured primary neurons. Neuroscience 146: 1-8.
30. Forman MS, Lee VM, Trojanowski JQ (2003) 'Unfolding' pathways in neurodegenerative disease. Trends Neurosci 26: 407-410.
31. Gass JN, Gifford NM, Brewer JW (2002) Activation of an unfolded protein response during differentiation of antibody-secreting B cells. J Biol Chem 277: 49047-49054.
32. Iwawaki T, Akai R (2006) Analysis of the XBP1 splicing mechanism using endoplasmic reticulum stress-indicators. Biochem Biophys Res Commun 350: 709-715.
33. Zhang K, Wong HN, Song B, Miller CN, Scheuner D, et al. (2005) The unfolded protein response sensor IRE1alpha is required at 2 distinct steps in B cell lymphopoiesis. J Clin Invest 115: 268-281.
34. Williams BL, Lipkin WI (2006) Endoplasmic reticulum stress and neurodegeneration in rats neonatally infected with borna disease virus. J Virol 80: 8613-8626.
35. Perry SW, Norman JP, Litzburg A, Zhang D, Dewhurst S, et al. (2005) HIV-1 transactivator of transcription protein induces mitochondrial hyperpolarization and synaptic stress leading to apoptosis. J Immunol 174: 4333-4344.
36. Matarrese P, Gambardella L, Cassone A, Vella S, Cauda R, et al. (2003) Mitochondrial membrane hyperpolarization hijacks activated T lymphocytes toward the apoptotic-prone phenotype: homeostatic mechanisms of HIV protease inhibitors. J Immunol 170: 6006-6015.
37. Nagy G, Koncz A, Perl A (2003) T cell activation-induced mitochondrial hyperpolarization is mediated by Ca2+- and redox-dependent production of nitric oxide. J Immunol 171: 5188-5197.
38. Perl A, Gergely P, Nagy G, Koncz A, Banki K (2004) Mitochondrial hyperpolarization: a checkpoint of T-cell life, death and autoimmunity. Trends Immunol 25: 360-367.
39. Norman JP, Perry SW, Kasischke KA, Volsky DJ, Gelbard HA (2007) 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 178: 869-876.
40. Bardo S, Cavazzini MG, Emptage N (2006) The role of the endoplasmic reticulum Ca2+ store in the plasticity of central neurons. Trends Pharmacol Sci 27: 78-84.
41. Solovyova N, Verkhratsky A (2002) Monitoring of free calcium in the neuronal endoplasmic reticulum: an overview of modern approaches. J Neurosci Methods 122: 1-12.
42. Palmer AE, Jin C, Reed JC, Tsien RY (2004) Bcl-2-mediated alterations in endoplasmic reticulum Ca2+ analyzed with an improved genetically encoded fluorescent sensor. Proc Natl Acad Sci U S A 101: 17404-17409.
43. Nath A, Psooy K, Martin C, Knudsen B, Magnuson DS, et al. (1996) Identification of a human immunodeficiency virus type 1 Tat epitope that is neuroexcitatory and neurotoxic. J Virol 70: 1475-1480.
44. New DR, Maggirwar SB, Epstein LG, Dewhurst S, Gelbard HA (1998) 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 273: 17852-17858.
45. Schroder M, Kaufman RJ (2005) ER stress and the unfolded protein response. Mutat Res 569: 29-63.
46. Cox JS, Shamu CE, Walter P (1993) Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 73: 1197-1206.
47. Ponting CP (2000) Proteins of the endoplasmic-reticulum-associated degradation pathway: domain detection and function prediction. Biochem J 351 Pt 2: 527-535.
48. Blobel G, Dobberstein B (1975) Transfer of proteins across membranes. I. Presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma. J Cell Biol 67: 835-851.
49. Brostrom CO, Brostrom MA (1998) Regulation of translational initiation during cellular responses to stress. Prog Nucleic Acid Res Mol Biol 58: 79-125.
50. Scheuner D, Song B, McEwen E, Liu C, Laybutt R, et al. (2001) Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol Cell 7: 1165-1176.
51. Altschafl BA, Beutner G, Sharma VK, Sheu SS, Valdivia HH (2007) The mitochondrial ryanodine receptor in rat heart: A pharmaco-kinetic profile. Biochim Biophys Acta 1768(7): 1784-1795.
52. Beutner G, Sharma VK, Lin L, Ryu SY, Dirksen RT, et al. (2005) Type 1 ryanodine receptor in cardiac mitochondria: transducer of excitation-metabolism coupling. Biochim Biophys Acta 1717: 1-10.
53. Arnaudeau S, Kelley WL, Walsh JV, Demaurex N (2001) Mitochondria recycle Ca(2+) to the endoplasmic reticulum and prevent the depletion of neighboring endoplasmic reticulum regions. J Biol Chem 276: 29430-29439.
54. Yankner BA, Duffy LK, Kirschner DA (1990) Neurotrophic and neurotoxic effects of amyloid beta protein: reversal by tachykinin neuropeptides. Science 250: 279-282.
55. Spillantini MG, Crowther RA, Jakes R, Hasegawa M, Goedert M (1998) alpha-Synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with lewy bodies. Proc Natl Acad Sci U S A 95: 6469-6473.
56. Yu CY, Hsu YW, Liao CL, Lin YL (2006) Flavivirus infection activates the XBP1 pathway of the unfolded protein response to cope with endoplasmic reticulum stress. J Virol 80: 11868-11880.
57. Li B, Gao B, Ye L, Han X, Wang W, et al. (2007) Hepatitis B virus X protein (HBx) activates ATF6 and IRE1-XBP1 pathways of unfolded protein response. Virus Res 124: 44-49.
58. Genis P, Jett M, Bernton EW, Boyle T, Gelbard HA, et al. (1992) Cytokines and arachidonic metabolites produced during human immunodeficiency virus (HIV)-infected macrophage-astroglia interactions: implications for the neuropathogenesis of HIV disease. J Exp Med 176: 1703-1718.
59. Gelbard HA, Dzenko K, DiLoreto D, del Cerro C, del Cerro M, et al. (1993) Neurotoxic effects of tumor necrosis factor in primary human neuronal cultures are mediated by activation of the glutamate AMPA receptor subtype: implications for AIDS neuropathogenesis. Dev Neurosci 15: 417-422.
60. Buriani A, Petrelli L, Facci L, Romano PG, Dal Tosso R, et al. (1999) Human immunodeficiency virus type 1 envelope glycoprotein gp120 induces tumor necrosis factor-alpha in astrocytes. J NeuroAIDS 2: 1-13.
61. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, et al. (2000) Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287: 664-666.
62. Hu P, Han Z, Couvillon AD, Kaufman RJ, Exton JH (2006) Autocrine tumor necrosis factor alpha links endoplasmic reticulum stress to the membrane death receptor pathway through IRE1alpha-mediated NF-kappaB activation and down-regulation of TRAF2 expression. Mol Cell Biol 26: 3071-84.
63. Griesbeck O, Baird GS, Campbell RE, Zacharias DA, Tsien RY (2001) Reducing the environmental sensitivity of yellow fluorescent protein. Mechanism and Applications. J Biol Chem 276: 29188-29194.
64. Brewer GJ, Torricelli JR, Evege EK, Price PJ (1993) Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J Neurosci Res 35: 567-576.
65. de Mesy Jensen KL, di Sant'Agnese PA (1983) A technique for electron microscopy on needle aspirate specimens. In: Bonfiglio TA, ed. The Cytopathologic Interpretation of Transthoracic Fine Needle Biopsies. Masson Monographs in Diagnostic Cytopathology, Vol. 4. pp 194.
66. Masliah E, Sisk A, Mallory M, Mucke L, Schenk D, et al. (1996) Comparison of neurodegenerative pathology in transgenic mice overexpressing V717F β-amyloid precursor protein and Alzheimer's disease. J Neurosci 16: 5795-5811.