Activation of kainate receptors sensitizes oligodendrocytes to complement attack

Journal of Neuroscience

Volumn 26, Issue 12, 2006, Pages 3220-3228

  Alberdi, Elena ^a   Sánchez Gómez, María Victoria ^a   Torre, Iratxe ^a   Domercq, María ^a   Pérez Samartín, Alberto ^a   Pérez Cerdá, Fernando ^a   Matute, Carlos ^a  

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

Author keywords

Calcium; Complement; Glutamate; Kainate receptors; Oligodendrocytes; Oxidative stress

Indexed keywords

AMPA RECEPTOR; CASPASE; COMPLEMENT MEMBRANE ATTACK COMPLEX; GLUTAMATE RECEPTOR; KAINIC ACID RECEPTOR; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RAT;

ANIMALS; ANIMALS, NEWBORN; ANTIOXIDANTS; CALCIUM; CELL DEATH; CELL MEMBRANE; CELLS, CULTURED; COMPLEMENT SYSTEM PROTEINS; DEMYELINATING AUTOIMMUNE DISEASES, CNS; DOSE-RESPONSE RELATIONSHIP, DRUG; GLUTAMIC ACID; MALE; NERVE FIBERS, MYELINATED; NEUROTOXINS; OLIGODENDROGLIA; OPTIC NERVE; OXIDATIVE STRESS; PATCH-CLAMP TECHNIQUES; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, KAINIC ACID;

EID: 33645219363     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3780-05.2006     Document Type: Article

References (51)

1. 2+ influx through AMPA or kainate receptors alone is sufficient to initiate excitotoxicity in cultured oligodendrocytes. Neurobiol Dis 9:234-243.
2. Appel SH, Bonstein MB (1964) The application of tissue culture to the study of experimental allergic encephalomyelitis. II. Serum factors responsible for demyelination. J Exp Med 119:303-312.
3. Barnett MH, Prineas JW (2004) Relapsing and remitting multiple sclerosis: pathology of the newly forming lesion. Ann Neurol 55:458-468.
4. Barnum SR (1995) Complement biosynthesis in the central nervous system. Crit Rev Oral Biol Med 6:132-146.
5. Bohana-Kashtan O, Ziporen L, Donin N, Kraus S, Fishelson Z (2004) Cell signals transduced by complement. Mol Immunol 41:583-597.
6. Choi DW (1998) Glutamate neurotoxicity and diseases of the nervous system. Neuron 1:623-634.
7. Compston DA, Morgan BP, Campbell AK, Wilkins P, Cole G, Thomas ND, Jasani B (1989) Immunocytochemical localization of the terminal complement complex in multiple sclerosis. Neuropathol Appl Neurobiol 15:307-316.
8. Follett PL, Rosenberg PA, Volpe JJ, Jensen FE (2000) NBQX attenuates excitotoxic injury in developing white matter. J Neurosci 20:9235-9241.
9. Gasque P, Dean YD, McGreal EP, VanBeek J, Morgan BP (2000) Complement components of the innate immune system in health and disease in the CNS. Immunopharmacology 49:171-186.
10. Hosokawa M, Klegeris A, Maguire J, McGeer PL (2003) Expression of complement messenger RNAs and proteins by human oligodendrocytes. Glia 42:417-423.
11. Kilgore KS, Schmid E, Shanley TP, Flory CM, Maheswari V, Tramontini NL, Cohen H, Ward PA, Friedl HP, Warren JS (1997) Sublytic concentrations of the membrane attack complex of complement induce endothelial interleukin-8 and monocyte chemoattractant protein-1 through nuclear factor-kappa B activation. Am J Pathol 150:2019-2031.
12. 2+ on the lytic process. J Immunol 138:1530-1536.
13. Levi-Strauss M, Mallat M (1987) Primary cultures of murine astrocytes produce C3 and factor B, two components of the alternative pathway of complement activation. J Immunol 139:2361-2366.
14. Linington C, Morgan BP, Scolding NJ, Wilkins P, Piddlesden S, Compston DA (1989) The role of complement in the pathogenesis of experimental allergic encephalomyelitis. Brain 112:895-911.
15. Lucchinetti C, Bruck W, Parisi J, Scheithauer B, Rodriguez M, Lassmann H (2000) Heterogeneity of multiple sclerosis lesions, implications for the pathogenesis of demyelination. Ann Neurol 47:707-717.
16. Matute C, Sánchez-Gómez MV, Martínez-Millán L, Miledi R (1997) Glutamate receptor-mediated toxicity in optic nerve oligodendrocytes. Proc Natl Acad Sci USA 94:8830-8835.
17. McCracken E, Fowler JH, Dewar D, Morrison S, McCulloch J (2002) Grey matter and white matter ischemic damage is reduced by the competitive AMPA receptor antagonist, SPD 502. J Cereb Blood Flow Metab 22:1090-1097.
18. McDonald JW, Althomsons SP, Hyrc KL, Choi DW, Goldberg MP (1998) Oligodendrocytes from forebrain are highly vulnerable to AMPA/kainate receptor-mediated excitotoxicity. Nat Med 4:291-297.
19. McGeer PL, Akiyama H, Itagaki S, McGeer EG (1989) Activation of the classical complement pathway in brain tissue of Alzheimer patients. Neurosci Lett 107:341-346.
20. Mead RJ, Singhrao SK, Neal JW, Lassmann H, Morgan BP (2002) The membrane attack complex of complement causes severe demyelination associated with acute axonal injury. J Immunol 168:458-465.
21. Mollnes TE, Vandvik B, Lea T, Vartdal F (1987) Intrathecal complement activation in neurological diseases evaluated by analysis of the terminal complement complex. J Neurol Sci 78:17-28.
22. Morgan BP (1999) Regulation of the complement membrane attack pathway. Crit Rev Immunol 19:173-198.
23. Muller-Eberhard HJ (1986) The membrane attack complex of complement. Annu Rev Immunol 4:503-528.
24. Nataf S, Carroll SL, Wetsel RA, Szalai AJ, Barnum SR (2000) Attenuation of experimental autoimmune demyelination in complement-deficient mice. J Immunol 165:5867-5873.
25. Nauta AJ, Daha MR, Tijsma O, van de Water B, Tedesco F, Roos A (2002) The membrane attack complex of complement induces caspase activation and apoptosis. Eur J Immunol 32:783-792.
26. Nicholls DG, Budd SL (2000) Mitochondria and neuronal survival. Physiol Rev 80:315-360.
27. Patel M, Day BJ, Crapo JD, Fridovich I, McNamara JO (1996) Requirement for superoxide in excitotoxic cell death. Neuron 16:345-355.
28. Pitt D, Werner P, Raine CS (2000) Glutamate excitotoxicity in a model of multiple sclerosis. Nat Med 6:67-70.
29. Pitt D, Nagelmeier IE, Wilson HC, Raine CS (2003) Glutamate uptake by oligodendrocytes: implications for excitotoxicity in multiple sclerosis. Neurology 61:1113-1120.
30. Prineas JW, Kwon EE, Cho ES, Sharer LR, Barnett MH, Oleszak EL, Hoffman B, Morgan BP (2001) Immunopathology of secondary-progressive multiple sclerosis. Ann Neurol 50:646-657.
31. Rus HG, Niculescu F, Shin ML (1996) Sublytic complement attack induces cell cycle in oligodendrocytes. J Immunol 15:4892-4900.
32. 2+ and ATP permeability thresholds in live cells attacked by complement. Immunology 93:601-609.
33. Sánchez-Gómez MV, Matute C (1999) AMPA and kainate receptors each mediate excitotoxicity in oligodendroglial cultures. Neurobiol Dis 6:475-485.
34. Sánchez-Gómez MV, Alberdi E, Ibarretxe G, Torre I, Matute C (2003) Caspase-dependent and caspase-independent oligodendrocyte death mediated by AMPA and kainate receptors. J Neurosci 23:9519-9528.
35. Schwab C, McGeer PL (2002) Complement activated C4d immunoreactive oligodendrocytes delineate small cortical plaques in multiple sclerosis. Exp Neurol 174:81-88.
36. Scolding NJ, Morgan BP, Compston DA (1998) The expression of complement regulatory proteins by adult human oligodendrocytes. J Neuroimmunol 1:69-75.
37. Shen Y, Meri S (2003) Yin and Yang, complement activation and regulation in Alzheimer's disease. Prog Neurobiol 70:463-472.
38. Singhrao SK, Neal JW, Morgan BP, Gasque P (1999) Increased complement biosynthesis by microglia and complement activation on neurons in Huntington's disease. Exp Neurol 159:362-376.
39. Smith T, Groom A, Zhu B, Turski L (2000) Autoimmune encephalomyelitis ameliorated by AMPA antagonists. Nat Med 6:62-66.
40. Soane L, Rus H, Niculescu F, Shin ML (1999) Inhibition of oligodendrocyte apoptosis by sublytic C5b-9 is associated with enhanced synthesis of bcl-2 and mediated by inhibition of caspase-3 activation. J Immunol 163:6132-6138.
41. Srinivasan R, Sailasuta N, Hurd R, Nelson S, Pelletier D (2005) Evidence of elevated glutamate in multiple sclerosis using magnetic resonance spectroscopy at 3 T. Brain 128:1016-1025.
42. Storch MK, Piddlesden S, Haltia M, Iivanainen M, Morgan P, Lassmann H (1998) Multiple sclerosis: in situ evidence for antibody- and complement-mediated demyelination. Ann Neurol 43:465-471.
43. Verkhratsky A, Steinhauser C (2000) Ion channels in glial cells. Brain Res Brain Res Rev 32:380-412.
44. Werner P, Pitt D, Raine CS (2001) Multiple sclerosis: altered glutamate homeostasis in lesions correlates with oligodendrocyte and axonal damage. Ann Neurol 50:169-180.
45. Whitney KD, Andrews PI, McNamara JO (1999) Immunoglobulin G and complement immunoreactivity in the cerebral cortex of patients with Rasmussen's encephalitis. Neurology 53:699-708.
46. Xiong Z, McNamara JO (2002) Fleeting activation of ionotropic glutamate receptors sensitizes cortical neurons to complement attack. Neuron 36:363-374.
47. Xu GY, Hughes MG, Ye Z, Hulsebosch CE, McAdoo DJ (2004) Concentrations of glutamate released following spinal cord injury kill oligodendrocytes in the spinal cord. Exp Neurol 187:329-336.
48. Yam P, Petz LD, Tourtellotte WW, Ma BI (1980) Measurement of complement components in cerebral spinal fluid by radioimmunoassay in patients with multiple sclerosis. Clin Immunol Immunopathol 17:492-505.
49. Yamada T, McGeer PL (1990) Oligodendroglial microtubular masses: an abnormality observed in some human neurodegenerative diseases. Neurosci Lett 120:163-166.
50. Yoshioka A, Bacskai B, Pleasure D (1996) Pathophysiology of oligodendroglial excitotoxicity. J Neurosci Res 46:427-437.
51. Yu SW, Wang H, Poitras MF, Coombs C, Bowers WJ, Federoff HJ, Poirier GG, Dawson TM, Dawson VL (2002) Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 297:259-263.