In vitro glutaminase regulation and mechanisms of glutamate generation in HIV-1-infected macrophage

Journal of Neurochemistry

Volumn 109, Issue 2, 2009, Pages 551-561

  Erdmann, Nathan ^a,b   Tian, Changhai ^a,b   Huang, Yunlong ^a,b   Zhao, Jianxing ^a,b   Herek, Shelley ^a,b   Curthoys, Norman ^c   Zheng, Jialin ^a,b  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b Department of Pharmacology/Experimental Neuroscience ^*  (United States)

^c Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Glutamate; Glutaminase; Human immunodeficiency virus 1 associated dementia; Macrophages

Indexed keywords

GLUTAMIC ACID; GLUTAMINASE; GLUTAMINE; MITOCHONDRIAL PROTEIN; RNA;

ARTICLE; CYTOSOL; DEMENTIA; DISEASE COURSE; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME INHIBITION; ENZYME LOCALIZATION; ENZYME RELEASE; EXCITOTOXICITY; EXTRACELLULAR SPACE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IN VITRO STUDY; MACROPHAGE; PRIORITY JOURNAL; PROTEIN ANALYSIS; RNA ANALYSIS;

AIDS DEMENTIA COMPLEX; CELLS, CULTURED; GLUTAMIC ACID; GLUTAMINASE; HIV INFECTIONS; HIV-1; HUMANS; MACROPHAGES;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 62649144579     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.05989.x     Document Type: Article

References (43)

1. Anderson E. R., Gendelman H. E. Xiong H. (2004) Memantine protects hippocampal neuronal function in murine human immunodeficiency virus type 1 encephalitis. J. Neurosci. 24, 7194 7198.
2. Baglietto-Vargas D., Lopez-Tellez J. F., Moreno-Gonzalez I., Gutierrez A. Aledo J. C. (2004) Segregation of two glutaminase isoforms in islets of Langerhans. Biochem. J. 381, 483 487.
3. Belmadani A., Zou J., Schipma M. J., Neafsey E. J. Collins M. A. (2001) Ethanol pre-exposure suppresses HIV-1 glycoprotein 120-induced neuronal degeneration by abrogating endogenous glutamate/Ca(2+)-mediated neurotoxicity. Neuroscience 104, 769 781.
4. Chen H. S. Lipton S. A. (2006) The chemical biology of clinically tolerated NMDA receptor antagonists. J. Neurochem. 97, 1611 1626.
5. Choi D. W. (1988) Glutamate neurotoxicity and diseases of the nervous system. Neuron 1, 623 634.
6. Curthoys N. P. Watford M. (1995) Regulation of glutaminase activity and glutamine metabolism. Annu. Rev. Nutr. 15, 133 159.
7. Cutler R. W. Dudzinski D. S. (1974) Regional changes in amino acid content in developing rat brain. J. Neurochem. 23, 1005 1009.
8. Droge W., Eck H. P., Betzler M. Naher H. (1987) Elevated plasma glutamate levels in colorectal carcinoma patients and in patients with acquired immunodeficiency syndrome (AIDS). Immunobiology 174, 473 479.
9. Elgadi K. M., Meguid R. A., Qian M., Souba W. W. Abcouwer S. F. (1999) Cloning and analysis of unique human glutaminase isoforms generated by tissue-specific alternative splicing. Physiol. Genomics 1, 51 62.
10. Erdmann N. W. N. Zheng J. (2006) Potentiation of excitotoxicity in HIV-1-associated Dementia and the significance of glutaminase. Clin. Neurosci. Res. 6, 315 328.
11. Erdmann N., Zhao J., Lopez A. L., Herek S., Curthoys N., Hexum T. D., Tsukamoto T., Ferraris D. Zheng J. (2007) Glutamate production by HIV-1 infected human macrophage is blocked by the inhibition of glutaminase. J. Neurochem. 102, 539 549.
12. Ferrarese C., Aliprandi A., Tremolizzo L., Stanzani L., De Micheli A., Dolara A. Frattola L. (2001) Increased glutamate in CSF and plasma of patients with HIV dementia. Neurology 57, 671 675.
13. Fonnum F. (1984) Glutamate: a neurotransmitter in mammalian brain. J. Neurochem. 42, 1 11.
14. Gendelman H. E., Orenstein J. M., Martin M. A. et al. (1988) Efficient isolation and propagation of human immunodeficiency virus on recombinant colony-stimulating factor 1-treated monocytes. J. Exp. Med. 167, 1428 1441.
15. Giulian D., Wendt E., Vaca K. Noonan C. A. (1993) The envelope glycoprotein of human immunodeficiency virus type 1 stimulates release of neurotoxins from monocytes. Proc. Natl Acad. Sci. USA 90, 2769 2773.
16. Hansson M. J., Persson T., Friberg H., Keep M. F., Rees A., Wieloch T. Elmer E. (2003) Powerful cyclosporin inhibition of calcium-induced permeability transition in brain mitochondria. Brain Res. 960, 99 111.
17. Holcomb T., Taylor L., Trohkimoinen J. Curthoys N. P. (2000) Isolation, characterization and expression of a human brain mitochondrial glutaminase cDNA. Brain Res. Mol. Brain Res. 76, 56 63.
18. Jiang Z., Piggee C., Heyes M. P., Murphy C., Quearry B., Bauer M., Zheng J., Gendelman H. E. Markey S. P. (2001) Glutamate is a mediator of neurotoxicity in secretions of activated HIV-1-infected macrophages. J. Neuroimmunol. 117, 97 107.
19. Kvamme E., Svenneby G., Hertz L. Schousboe A. (1982) Properties of phosphate activated glutaminase in astrocytes cultured from mouse brain. Neurochem. Res. 7, 761 770.
20. Laake J. H., Takumi Y., Eidet J., Torgner I. A., Roberg B., Kvamme E. Ottersen O. P. (1999) Postembedding immunogold labelling reveals subcellular localization and pathway-specific enrichment of phosphate activated glutaminase in rat cerebellum. Neuroscience 88, 1137 1151.
21. Masson J., Darmon M., Conjard A. et al. (2006) Mice lacking brain/kidney phosphate-activated glutaminase have impaired glutamatergic synaptic transmission, altered breathing, disorganized goal-directed behavior and die shortly after birth. J. Neurosci. 26, 4660 4671.
22. McCall A., Glaeser B. S., Millington W. Wurtman R. J. (1979) Monosodium glutamate neurotoxicity, hyperosmolarity, and blood-brain barrier dysfunction. Neurobehav. Toxicol. 1, 279 283.
23. Mock B., Kozak C., Seldin M. F. et al. (1989) A glutaminase (gis) gene maps to mouse chromosome 1, rat chromosome 9, and human chromosome 2. Genomics 5, 291 297.
24. Newcomb R., Sun X., Taylor L., Curthoys N. Giffard R. G. (1997) Increased production of extracellular glutamate by the mitochondrial glutaminase following neuronal death. J. Biol. Chem. 272, 11276 11282.
25. Nicklas W. J., Zeevalk G. Hyndman A. (1987) Interactions between neurons and glia in glutamate/glutamine compartmentation. Biochem. Soc. Trans. 15, 208 210.
26. Ollenschlager G., Jansen S., Schindler J., Rasokat H., Schrappe-Bacher M. Roth E. (1988) Plasma amino acid pattern of patients with HIV infection. Clin. Chem. 34, 1787 1789.
27. Olney J. W. (1971) Glutamate-induced neuronal necrosis in the infant mouse hypothalamus. An electron microscopic study. J. Neuropathol. Exp. Neurol. 30, 75 90.
28. Orrego F. Villanueva S. (1993) The chemical nature of the main central excitatory transmitter: a critical appraisal based upon release studies and synaptic vesicle localization. Neuroscience 56, 539 555.
29. Peng H., Erdmann N., Whitney N., Dou H., Gorantla S., Gendelman H. E., Ghorpade A. Zheng J. (2006) HIV-1-infected and/or immune activated macrophages regulate astrocyte SDF-1 production through IL-1beta. Glia 54, 619 629.
30. Piani D., Frei K., Do K., Cuenod M. Fontana A. (1991) Murine brain macrophages induce NMDA receptor mediated neurotoxicity in vitro by secreting glutamate. Neurosci. Lett. 133, 159 162.
31. Porter D., Hansen W. R., Taylor L. Curthoys N. P. (1995) Differential expression of multiple glutaminase mRNAs in LLC-PK1-F+ cells. Am. J. Physiol. 269, F363 F373.
32. Porter L. D., Ibrahim H., Taylor L. Curthoys N. P. (2002) Complexity and species variation of the kidney-type glutaminase gene. Physiol. Genomics 9, 157 166.
33. Pulliam L., Clarke J. A., McGuire D. McGrath M. S. (1994) Investigation of HIV-infected macrophage neurotoxin production from patients with AIDS dementia. Adv. Neuroimmunol. 4, 195 198.
34. Shapiro R. A., Haser W. G. Curthoys N. P. (1985) The orientation of phosphate-dependent glutaminase on the inner membrane of rat renal mitochondria. Arch. Biochem. Biophys. 243, 1 7.
35. Shapiro R. A., Farrell L., Srinivasan M. Curthoys N. P. (1991) Isolation, characterization, and in vitro expression of a cDNA that encodes the kidney isoenzyme of the mitochondrial glutaminase. J. Biol. Chem. 266, 18792 18796.
36. Szeliga M., Matyja E., Obara M., Grajkowska W., Czernicki T. Albrecht J. (2008) Relative expression of mRNAS coding for glutaminase isoforms in CNS tissues and CNS tumors. Neurochem. Res. 33, 808 813.
37. Tian C., Erdmann N., Zhao J., Cao Z., Peng H. Zheng J. (2008a) HIV-infected macrophages mediate neuronal apoptosis through mitochondrial glutaminase. J. Neurochem. 105, 994 1005.
38. Tian C., Gao P., Zheng Y., Yue W., Wang X., Jin H. Chen Q. (2008b) Redox status of thioredoxin-1 (TRX1) determines the sensitivity of human liver carcinoma cells (HepG2) to arsenic trioxide-induced cell death. Cell Res. 18, 458 471.
39. Ward H. K., Thanki C. M. Bradford H. F. (1983) Glutamine and glucose as precursors of transmitter amino acids: ex vivo studies. J. Neurochem. 40, 855 860.
40. Wurdig S. Kugler P. (1991) Histochemistry of glutamate metabolizing enzymes in the rat cerebellar cortex. Neurosci. Lett. 130, 165 168.
41. Yawata I., Takeuchi H., Doi Y., Liang J., Mizuno T. Suzumura A. (2008) Macrophage-induced neurotoxicity is mediated by glutamate and attenuated by glutaminase inhibitors and gap junction inhibitors. Life Sci. 82, 1111 1116.
42. Zhao J., Lopez A. L., Erichsen D., Herek S., Cotter R. L., Curthoys N. P. 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.
43. Zink W. E., Zheng J., Persidsky Y., Poluektova L. Gendelman H. E. (1999) The neuropathogenesis of HIV-1 infection. FEMS Immunol. Med. Microbiol. 26, 233 241.