IL-1β and TNF-α induce neurotoxicity through glutamate production: A potential role for neuronal glutaminase

Journal of Neurochemistry

Volumn 125, Issue 6, 2013, Pages 897-908

  Ye, Ling ^a,b,c   Huang, Yunlong ^c   Zhao, Lixia ^c   Li, Yuju ^c   Sun, Lijun ^c   Zhou, You ^d   Qian, Guanxiang ^a   Zheng, Jialin C ^b,c,e  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

^c UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^d UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^e UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

glutamate; glutaminase; inflammation; neurotoxicity

Indexed keywords

BETA TUBULIN; BETA TUBULIN III; GLUTAMIC ACID; GLUTAMINASE; INTERLEUKIN 1BETA; KIDNEY TYPE GLUTAMINASE; MICROTUBULE ASSOCIATED PROTEIN 2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

AMINO ACID SYNTHESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL LOSS; CELL SIZE; CELL STIMULATION; CELL VIABILITY; CONTROLLED STUDY; CYTOSOL; EMBRYO; ENZYME LOCALIZATION; ENZYME RELEASE; EXTRACELLULAR FLUID; FETUS; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NERVE CELL LESION; NERVE CELL NECROSIS; NEUROPATHOLOGY; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; UPREGULATION; VIRUS ENCEPHALITIS;

ANIMALS; CELL DEATH; CEREBRAL CORTEX; CYTOSOL; ENCEPHALITIS, VIRAL; EXTRACELLULAR SPACE; GLUTAMIC ACID; GLUTAMINASE; HIV-1; HUMANS; INTERLEUKIN-1BETA; INTRACELLULAR SPACE; MALE; MICE; MICE, SCID; MITOCHONDRIA; NEURONS; PRIMARY CELL CULTURE; RATS; RATS, SPRAGUE-DAWLEY; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

HUMAN IMMUNODEFICIENCY VIRUS 1; MAMMALIA; MURINAE; RATTUS;

EID: 84878767675     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12263     Document Type: Article

References (48)

1. Baglietto-Vargas D., Lopez-Tellez J. F., Moreno-Gonzalez I., Gutierrez A., and, Aledo J. C., (2004) Segregation of two glutaminase isoforms in islets of Langerhans. Biochem. J. 381, 483-487.
2. Bender L. M., Morgan M. J., Thomas L. R., Liu Z. G., and, Thorburn A., (2005) The adaptor protein TRADD activates distinct mechanisms of apoptosis from the nucleus and the cytoplasm. Cell Death Differ. 12, 473-481.
3. Benveniste H., (2009) Glutamate, microdialysis, and cerebral ischemia: lost in translation? Anesthesiology 110, 422-425.
4. Block M. L., Zecca L., and, Hong J. S., (2007) Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat. Rev. Neurosci. 8, 57-69.
5. Boutin H., LeFeuvre R. A., Horai R., Asano M., Iwakura Y., and, Rothwell N. J., (2001) Role of IL-1alpha and IL-1beta in ischemic brain damage. J. Neurosci. 21, 5528-5534.
6. Chao C. C., Hu S., Ehrlich L., and, Peterson P. K., (1995) Interleukin-1 and tumor necrosis factor-alpha synergistically mediate neurotoxicity: involvement of nitric oxide and of N-methyl-D-aspartate receptors. Brain Behav. Immun. 9, 355-365.
7. Constantino A. A., Huang Y., Zhang H., Wood C., and, Zheng J. C., (2011) HIV-1 clade B and C isolates exhibit differential replication: relevance to macrophage-mediated neurotoxicity. Neurotox. Res. 20, 277-288.
8. Dohmen C., Kumura E., Rosner G., Heiss W. D., and, Graf R., (2005) Extracellular correlates of glutamate toxicity in short-term cerebral ischemia and reperfusion: a direct in vivo comparison between white and gray matter. Brain Res. 1037, 43-51.
9. Erdmann N. B., Whitney N. P., and, Zheng J., (2006) Potentiation of excitotoxicity in HIV-1 associated dementia and the significance of glutaminase. Clin. Neurosci. Res. 6, 315-328.
10. Erdmann N., Tian C., Huang Y., Zhao J., Herek S., Curthoys N., and, Zheng J., (2009) In vitro glutaminase regulation and mechanisms of glutamate generation in HIV-1-infected macrophage. J. Neurochem. 109, 551-561.
11. Esser R., Glienke W., von Briesen H., Rubsamen-Waigmann H., and, Andreesen R., (1996) Differential regulation of proinflammatory and hematopoietic cytokines in human macrophages after infection with human immunodeficiency virus. Blood 88, 3474-3481.
12. Gao P., Tchernyshyov I., Chang T. C., et al,. (2009) c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism. Nature 458, 762-765.
13. Gardoni F., Boraso M., Zianni E., Corsini E., Galli C. L., Cattabeni F., Marinovich M., Di Luca M., and, Viviani B., (2011) Distribution of interleukin-1 receptor complex at the synaptic membrane driven by interleukin-1beta and NMDA stimulation. J. Neuroinflammation 8, 14.
14. Guo H., Jin Y. X., Ishikawa M., Huang Y. M., van der Meide P. H., Link H., and, Xiao B. G., (1998) Regulation of beta-chemokine mRNA expression in adult rat astrocytes by lipopolysaccharide, proinflammatory and immunoregulatory cytokines. Scand. J. Immunol. 48, 502-508.
15. Holcomb T., Taylor L., Trohkimoinen J., and, Curthoys N. P., (2000) Isolation, characterization and expression of a human brain mitochondrial glutaminase cDNA. Brain Res. Mol. Brain Res. 76, 56-63.
16. Hu S., Sheng W. S., Peterson P. K., and, Chao C. C., (1995) Differential regulation by cytokines of human astrocyte nitric oxide production. Glia 15, 491-494.
17. Hu S., Peterson P. K., and, Chao C. C., (1997) Cytokine-mediated neuronal apoptosis. Neurochem. Int. 30, 427-431.
18. Huang Y., Erdmann N., Peng H., Zhao Y., and, Zheng J., (2005) The role of TNF related apoptosis-inducing ligand in neurodegenerative diseases. Cell. Mol. Immunol. 2, 113-122.
19. Huang Y., Zhao L., Jia B., Wu L., Li Y., Curthoys N., and, Zheng J. C., (2011) Glutaminase dysregulation in HIV-1-infected human microglia mediates neurotoxicity: relevant to HIV-1-associated neurocognitive disorders. J. Neurosci. 31, 15195-15204.
20. Jiang Z. G., Piggee C., Heyes M. P., Murphy C., Quearry B., Bauer M., Zheng J., Gendelman H. E., and, Markey S. P., (2001) Glutamate is a mediator of neurotoxicity in secretions of activated HIV-1-infected macrophages. J. Neuroimmunol. 117, 97-107.
21. Kanellopoulos G. K., Xu X. M., Hsu C. Y., Lu X., Sundt T. M., and, Kouchoukos N. T., (2000) White matter injury in spinal cord ischemia: protection by AMPA/kainate glutamate receptor antagonism. Stroke 31, 1945-1952.
22. Killestein J., Kalkers N. F., and, Polman C. H., (2005) Glutamate inhibition in MS: the neuroprotective properties of riluzole. J. Neurol. Sci. 233, 113-115.
23. Komuro H., and, Rakic P., (1996) Intracellular Ca2+ fluctuations modulate the rate of neuronal migration. Neuron 17, 275-285.
24. Leist M., and, Nicotera P., (1998) Apoptosis, excitotoxicity, and neuropathology. Exp. Cell Res. 239, 183-201.
25. LoTurco J. J., Blanton M. G., and, Kriegstein A. R., (1991) Initial expression and endogenous activation of NMDA channels in early neocortical development. J. Neurosci. 11, 792-799.
26. Maezawa I., and, Jin L. W., (2010) Rett syndrome microglia damage dendrites and synapses by the elevated release of glutamate. J. Neurosci. 30, 5346-5356.
27. McEntee W. J., and, Crook T. H., (1993) Glutamate: its role in learning, memory, and the aging brain. Psychopharmacology 111, 391-401.
28. Meldrum B. S., (2000) Glutamate as a neurotransmitter in the brain: review of physiology and pathology. J. Nutr. 130, 1007S-1015S.
29. Newcomb R., Sun X., Taylor L., Curthoys N., and, Giffard R. G., (1997) Increased production of extracellular glutamate by the mitochondrial glutaminase following neuronal death. J. Biol. Chem. 272, 11276-11282.
30. Peng H., Erdmann N., Whitney N., Dou H., Gorantla S., Gendelman H. E., Ghorpade A., and, Zheng J., (2006) HIV-1-infected and/or immune activated macrophages regulate astrocyte SDF-1 production through IL-1beta. Glia 54, 619-629.
31. Persidsky Y., Limoges J., McComb R., et al,. (1996) Human immunodeficiency virus encephalitis in SCID mice. Am. J. Pathol. 149, 1027-1053.
32. Porter L. D., Ibrahim H., Taylor L., and, Curthoys N. P., (2002) Complexity and species variation of the kidney-type glutaminase gene. Physiol. Genomics 9, 157-166.
33. Rao V. L., Baskaya M. K., Dogan A., Rothstein J. D., and, Dempsey R. J., (1998) Traumatic brain injury down-regulates glial glutamate transporter (GLT-1 and GLAST) proteins in rat brain. J. Neurochem. 70, 2020-2027.
34. Smith J. A., Das A., Ray S. K., and, Banik N. L., (2011) Role of pro-inflammatory cytokines released from microglia in neurodegenerative diseases. Brain Res. Bull. 87, 10-20.
35. Takikita S., Takano T., Narita T., Takikita M., Ohno M., and, Shimada M., (2001) Neuronal apoptosis mediated by IL-1 beta expression in viral encephalitis caused by a neuroadapted strain of the mumps virus (Kilham Strain) in hamsters. Exp. Neurol. 172, 47-59.
36. Tian C., Erdmann N., Zhao J., Cao Z., Peng H., and, Zheng J., (2008) HIV-infected macrophages mediate neuronal apoptosis through mitochondrial glutaminase. J. Neurochem. 105, 994-1005.
37. Tian C., Sun L., Jia B., Ma K., Curthoys N., Ding J., and, Zheng J., (2012) Mitochondrial glutaminase release contributes to glutamate-mediated neurotoxicity during human immunodeficiency virus-1 infection. J. Neuroimmune Pharmacol. 7, 619-628.
38. Van Eldik L. J., Thompson W. L., Ralay Ranaivo H., Behanna H. A., and, Martin Watterson D., (2007) Glia proinflammatory cytokine upregulation as a therapeutic target for neurodegenerative diseases: function-based and target-based discovery approaches. Int. Rev. Neurobiol. 82, 277-296.
39. Viviani B., Bartesaghi S., Corsini E., Galli C. L., and, Marinovich M., (2004) Cytokines role in neurodegenerative events. Toxicol. Lett. 149, 85-89.
40. Wang J. B., Erickson J. W., Fuji R., et al,. (2010) Targeting mitochondrial glutaminase activity inhibits oncogenic transformation. Cancer Cell 18, 207-219.
41. Xu G. Y., Hughes M. G., Ye Z., Hulsebosch C. E., and, McAdoo D. J., (2004) Concentrations of glutamate released following spinal cord injury kill oligodendrocytes in the spinal cord. Exp. Neurol. 187, 329-336.
42. Zhang R., Yamada J., Hayashi Y., Wu Z., Koyama S., and, Nakanishi H., (2008) Inhibition of NMDA-induced outward currents by interleukin-1beta in hippocampal neurons. Biochem. Biophys. Res. Commun. 372, 816-820.
43. Zhao J., Lopez A. L., Erichsen D., Herek S., Cotter R. L., Curthoys N. P., and, Zheng J., (2004) Mitochondrial glutaminase enhances extracellular glutamate production in HIV-1-infected macrophages: linkage to HIV-1 associated dementia. J. Neurochem. 88, 169-180.
44. Zhao L., Huang Y., Tian C., Taylor L., Curthoys N., Wang Y., Vernon H., and, Zheng J., (2012) Interferon-alpha regulates glutaminase 1 promoter through STAT1 phosphorylation: relevance to HIV-1 associated neurocognitive disorders. PLoS ONE 7, e32995.
45. Zheng J., Thylin M. R., Ghorpade A., et al,. (1999) Intracellular CXCR4 signaling, neuronal apoptosis and neuropathogenic mechanisms of HIV-1-associated dementia. J. Neuroimmunol. 98, 185-200.
46. Zheng J., Thylin M. R., Cotter R. L., et al,. (2001) HIV-1 infected and immune competent mononuclear phagocytes induce quantitative alterations in neuronal dendritic arbor: relevance for HIV-1-associated dementia. Neurotox. Res. 3, 443-459.
47. Zindler E., and, Zipp F., (2011) Neuronal injury in chronic CNS inflammation. Best Pract. Res. Clin. Anaesthesiol. 24, 551-562.
48. Zoia C. P., Tagliabue E., Isella V., Begni B., Fumagalli L., Brighina L., Appollonio I., Racchi M., and, Ferrarese C., (2005) Fibroblast glutamate transport in aging and in AD: correlations with disease severity. Neurobiol. Aging 26, 825-832.