System xc- and glutamate transporter inhibition mediates microglial toxicity to oligodendrocytes

Journal of Immunology

Volumn 178, Issue 10, 2007, Pages 6549-6556

  Domercq, María ^a   Sánchez Gómez, María Victoria ^a   Sherwin, Catherine ^b   Etxebarria, Estibaliz ^a   Fern, Robert ^b   Matute, Carlos ^a  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; ANTIPORTER; CYSTINE; GLUTAMATE TRANSPORTER; GLUTAMIC ACID; KAINIC ACID RECEPTOR; LIPOPOLYSACCHARIDE; AUTACOID; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ARTICLE; BRAIN DISEASE; CELL ACTIVATION; CELL CULTURE; CELL DAMAGE; CELL DEATH; CELL DISRUPTION; CELL SWELLING; CYTOTOXICITY; GLIA CELL; HOMEOSTASIS; MICROGLIA; MITOCHONDRION; NERVE FIBER; NONHUMAN; OLIGODENDROGLIA; OPTIC NERVE; PATHOGENESIS; PRIORITY JOURNAL; RAT; WHITE MATTER; ANIMAL; COCULTURE; DRUG ANTAGONISM; EXCITATORY POSTSYNAPTIC POTENTIAL; METABOLISM; PATHOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

AMINO ACID TRANSPORT SYSTEM X-AG; ANIMALS; CELL DEATH; CELLS, CULTURED; COCULTURE TECHNIQUES; CYSTINE; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; HOMEOSTASIS; INFLAMMATION MEDIATORS; LIPOPOLYSACCHARIDES; MICROGLIA; OLIGODENDROGLIA; OPTIC NERVE; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES;

EID: 34248174912     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.178.10.6549     Document Type: Article

References (49)

1. Merrill, J. E., L. J. Ignarro, M. P. Sherman, J. Melinek, and T. E. Lane. 1993. Microglial cell cytotoxicity of oligodendrocytes is mediated through nitric oxide. J. Immunol. 151: 2132-2141.
2. - in the macrophage-induced glutamate-dependent cytotoxicity to neurons. J. Immunol. 152: 3578-3585.
3. Bezzi, P., M. Domercq, L. Brambilla, R. Galli, D. Schols, E. De Clercq, A. Vescovi, G. Bagetta, G. Kollias, J. Meldolesi, and A. Volterra. 2001. CXCR4-activated astrocyte glutamate release via TNFα: amplification by microglia triggers neurotoxicity. Nat. Neurosci. 4: 702-710.
4. Block, M. L., and J. S. Hong. 2005. Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog. Neurobiol. 76: 77-98.
5. Schwartz, M., O. Butovsky, W. Brack, and U. K. Hanisch. 2006. Microglial phenotype: is the commitment reversible? Trends Neurosci. 29: 68-74.
6. Hartung, H. P., S. Jung, G. Stoll, J. Zielasek, B. Schmidt, J. J. Archelos, and K. V. Toyka. 1992. Inflammatory mediators in demyelinating disorders of the CNS and PNS. J. Neuroimmunol. 40: 197-210.
7. Carson, M. J. 2002. Microglia as liaisons between the immune and central nervous systems: functional implications for multiple sclerosis. Glia 40: 218-231.
8. Robbins, D. S., Y. Shirazi, B. E. Drysdale, A. Lieberman, H. S. Shin, and M. L. Shin. 1987. Production of cytotoxic factor for oligodendrocytes by stimulated astrocytes. J. Immunol. 139: 2593-2597.
9. Pang, Y., Z. Cai, and P. G. Rhodes. 2000. Effects of lipopolysaccharide on oligodendrocyte progenitor cells are mediated by astrocytes and microglia. J. Neurosci. Res. 62: 510-520.
10. Molina-Holgado, E., J. M. Vela, A. Arevalo-Martin, and C. Guaza. 2001. LPS/ IFN-γ cytotoxicity in oligodendroglial cells: role of nitric oxide and protection by the anti-inflammatory cytokine IL-10. Eur. J. Neurosci. 13: 493-502.
11. Lehnardt, S., C. Lachance, S. Patrizi, S. Lefebvre, P. L. Follett, F. E. Jensen, P. A. Rosenberg, J. J. Volpe, and T. Vartanian. 2002. The toll-like receptor TLR4 is necessary for lipopolysaccharide-induced oligodendrocyte injury in the CNS. J. Neurosci. 22: 2478-2486.
12. Sherwin, C., and R. Fern. 2005. Acute lipopolysaccharide-mediated injury in neonatal white matter glia: role of TNF-α, IL-1β, and calcium. J. Immunol. 175: 155-161.
13. Li, J., O. Baud, T. Vartanian, J. J. Volpe, and P. A. Rosenberg. 2005. Peroxynitrite generated by inducible nitric oxide synthase and NADPH oxidase mediates microglial toxicity to oligodendrocytes. Proc. Natl. Acad Sci. USA 102: 9936-9941.
14. Heppner, F. L., M. Greter, D. Marino, J. Falsig, G. Raivich, N. Hovelmeyer, A. Waisman, T. Rulicke, M. Prinz, J. Priller, et al. 2005. Experimental autoimmune encephalomyelitis repressed by microglial paralysis. Nat. Med. 11: 146-152.
15. Yoshioka, A., B. Bacskai, and D. Pleasure. 1996. Pathophysiology of oligodendroglial excitotoxicity. J. Neurosci. Res. 46: 427-437.
16. Matute, C., M. V. Sánchez-Gómez, L. Martínez- Millán, and R. Miledi. 1997. Glutamate receptor-mediated toxicity in optic nerve oligodendrocytes. Proc. Natl. Acad. Sci. USA 94: 8830-8835.
17. McDonald, J. W., S. P. Althomsons, K. L. Hyrc, D. W. Choi, and M. P. Goldberg. 1998. Oligodendrocytes from forebrain are highly vulnerable to AMPA/kainate receptor-mediated excitotoxicity, Nat. Med. 4: 291-297.
18. Fern, R., and T. Moller. 2000. Rapid ischemic cell death in immature oligodendrocytes: a fatal glutamate release feedback loop. J. Neurosci. 20: 34-42.
19. Hardin-Pouzet, H., M. Krakowski, L. Bourbonniere, M. Didier-Bazes, E. Tran, and T. Owens. 1997. Glutamate metabolism is down-regulated in astrocytes during experimental allergic encephalomyelitis. Glia 20: 79-85.
20. Ohgoh, M., T. Hanada, T. Smith, T. Hashimoto, M. Ueno, Y. Yamanishi, M. Watanabe, and Y. Nishizawa. 2002. Altered expression of glutamate transporters in experimental autoimmune encephalomyelitis. J. Neuroimmunol. 125: 170-178.
21. Pitt, D., P. Werner, and C. S. Raine. 2000. Glutamate excitotoxicity in a model of multiple sclerosis. Nat. Med. 6: 67-70.
22. Smith, T., A. Groom, B. Zhu, and L. Turski. 2000. Autoimmune encephalomy-elitis ameliorated by AMPA antagonists. Nat. Med. 6: 62-66.
23. Matute, C., E. Alberdi, M. Domercq, F. Pérez-Cerdá, A. Pérez-Samartín, and M. V. Sánchez-Gómez. 2001. The link between excitotoxic oligodendroglial death and demyelinating diseases. Trends Neurosci. 24: 224-230.
24. Srinivasan, R., N. Sailasuta, R. Hurd, S. Nelson, and D. Pelletier. 2005. Evidence of elevated glutamate in multiple sclerosis using magnetic resonance spectroscopy at 3 T. Brain 128: 1016-1025.
25. McBean, G. J. 2002. Cerebral cystine uptake: a tale of two transporters. Trends Pharmacol. Sci. 23: 299-302.
26. Sato, H., M. Tamba, T. Ishii, and S. Bannai. 1999. Cloning and expression of a plasma membrane cystine/glutamate exchange transporter composed of two distinct proteins. J. Biol. Chem. 274: 11455-11458.
27. Sato, H., K. Kuriyama-Matsumura, T. Hashimoto, H. Sasaki, H. Wang, T. Ishii, G. E. Mann, and S. Bannai. 2001. Effect of oxygen on induction of the cystine transporter by bacterial lipopolysaccharide in mouse peritoneal macrophages. J. Biol. Chem. 276: 10407-10412.
28. - and apolipoprotein E expressed by microglia have opposite effects on the neurotoxicity of amyloid-β peptide 1-40. J. Neurosci. 26: 3345-3356.
29. Barres, B. A., I. K. Hart, H. S. Coles, J. F. Burne, J. T. Voyvodic, W. D. Richardson, and M. C. Raff. 1992. Cell death and control of cell survival in the oligodendrocyte lineage. Cell 70: 31-46.
30. Oka, A., M. J. Belliveau, P. A. Rosenberg, and J. J. Volpe. 1993. Vulnerability of oligodendroglia to glutamate: pharmacology, mechanisms, and prevention. J. Neurosci. 13: 1441-1453.
31. Domercq, M., M. V. Sánchez-Gómez, P. Areso, and C. Matute. 1999. Expression of glutamate transporters in rat optic nerve oligodendrocytes. Eur. J. Neurosci. 11: 2226-2236.
32. Domercq, M., E. Etxebarria, A. Pérez-Samartín, and C. Matute. 2005. Excitotoxic oligodendrocyte death and axonal damage induced by glutamate transporter inhibition. Glia 52: 36-46.
33. Szumlinski, K. K., M. H. Dehoff, S. H. Kang, K. A. Frys, K. D. Lominac, M. Klugmann, J. Rohrer, W. Griffin, 3rd, S. Toda, N. P. Champtiaux, et al. 2004. Homer proteins regulate sensitivity to cocaine. Neuron 43: 401-413.
34. +-dependent glutamate transport. J. Neurosci. 19: RC16.
35. Patel, M., B. J. Day, J. D. Crapo, I. Fridovich, and J. O. McNamara. 1996. Requirement for superoxide in excitotoxic cell death. Neuron 16: 345-355.
36. Sánchez-Gómez, M. V., E. Alberdi, G. Ibarretxe, I. Torre, and C. Matute. 2003. Caspase-dependent and caspase-independent oligodendrocyte death mediated by AMPA and kainate receptors. J. Neurosci. 23: 9519-9528.
37. 2+ influx at a key point in white matter development. J. Neuropathol. Exp. Neurol. 63: 856-871.
38. Wilke, S., M. Salter, M. R. Thomas, N. Allcock, and R. Fern. 2004. Mechanism of acute ischemic injury of oligodendroglia in early myelinating white matter: the importance of astrocyte injury and glutamate release. J. Neuropathol. Exp. Neurol. 63: 872-881.
39. Salter, M., and R. Fern. 2005. NMDA receptors are expressed in developing oligodendrocyte processes and mediate injury. Nature 438: 1167-1171.
40. Pitt, D., I. E. Nagelmeier, H. C. Wilson, and C. S. Raine. 2003. Glutamate uptake by oligodendrocytes: implications for excitotoxicity in multiple sclerosis. Neurology 61: 1113-1120.
41. Takahashi, J. L., F. Giuliani, C. Power, Y. Imai, and V. W. Yong. 2003. Interleukin-1β promotes oligodendrocyte death through glutamate excitotoxicity. Ann. Neurol. 53: 588-595.
42. Romera, C., O. Hurtado, S. H. Botella, I. Lizasoain, A. Cardenas, P. Fernandez-Tome, J. C. Leza, P. Lorenzo, and M. A. Moro. 2004. In vitro ischemic tolerance involves upregulation of glutamate transport partly mediated by the TACE/ ADAM17-tumor necrosis factor-α pathway. J. Neurosci. 24: 1350-1357.
43. Trotti, D., D. Rossi, O. Gjesdal, L. M. Levy, G. Racagni, N. C. Danbolt, and A. Volterra. 1996. Peroxynitrite inhibits glutamate transporter subtypes. J. Biol. Chem. 271: 5976-5979.
44. Werner, P., D. Pitt, and C. S. Raine. 2001. Multiple sclerosis: altered glutamate homeostasis in lesions correlates with oligodendrocyte and axonal damage. Ann. Neurol. 50: 169-180.
45. Westall, F. C., A. Hawkins, G. W. Ellison, and L. W. Myers. 1980. Abnormal glutamic acid metabolism in multiple sclerosis. J. Neurol. Sci. 47: 353-364.
46. Korn, T., T. Magnus, and S. Jung. 2005. Autoantigen specific T cells inhibit glutamate uptake in astrocytes by decreasing expression of astrocytic glutamate transporter GLAST: a mechanism mediated by tumor necrosis factor-α. FASEB J. 19: 1878-1880.
47. Baker, D. A., Z. X. Xi, H. Shen, C. J. Swanson, and P. W. Kalivas. 2002. The origin and neuronal function of in vivo nonsynaptic glutamate. J. Neurosci. 22: 9134-9141.
48. Barger, S. W., and A. S. Basile. 2001. Activation of microglia by secreted amyloid precursor protein evokes release of glutamate by cystine exchange and attenuates synaptic function. J. Neurochem. 76: 846-854.
49. Espey, M. G., Y. Kustova, Y. Sei, and A. S. Basile. 1998. Extracellular glutamate levels are chronically elevated in the brains of LP-BM5-infected mice: a mechanism of retrovirus-induced encephalopathy. J. Neurochem. 71: 2079-2087.