Tumour necrosis factor alpha induces rapid reduction in AMPA receptor-mediated calcium entry in motor neurones by increasing cell surface expression of the GluR2 subunit: Relevance to neurodegeneration

Journal of Neurochemistry

Volumn 113, Issue 3, 2010, Pages 692-703

  Rainey Smith, Stephanie R ^a   Andersson, David A ^a   Williams, Robert J ^a   Rattray, Marcus ^b  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF READING   (United Kingdom)

Author keywords

AMPAR; Amyotrophic lateral sclerosis; Calcium permeable; Excitotoxicity; Trafficking; Tumour necrosis factor alpha

Indexed keywords

AMPA RECEPTOR; CALCIUM; GLUTAMATE RECEPTOR 1; GLUTAMATE RECEPTOR 2; PHOSPHATIDYLINOSITOL 3 KINASE; SYNAPTOPHYSIN; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA RECEPTOR;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CELL DEATH; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; EMBRYO; EXCITOTOXICITY; FEMALE; MOTONEURON; MOUSE; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SYNAPSE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; BIOTINYLATION; BLOTTING, WESTERN; CALCIUM; CALCIUM SIGNALING; CELL SURVIVAL; CELLS, CULTURED; EXCITATORY AMINO ACID AGONISTS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; KAINIC ACID; MICE; MOTOR NEURONS; NERVE DEGENERATION; NEUROPROTECTIVE AGENTS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PREGNANCY; RECEPTORS, AMPA; RECEPTORS, CELL SURFACE; RECEPTORS, TUMOR NECROSIS FACTOR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPECTROMETRY, FLUORESCENCE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 77950633637     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06634.x     Document Type: Article

References (69)

1. 2+ accumulation. Proc. Natl Acad. Sci. USA 92, 9328 9332.
2. Beattie E. C., Stellwagen D., Morishita W., Bresnahan J. C., Ha B. K., Von Zastrow M., Beattie M. S. Malenka R. C. (2002) Control of synaptic strength by glial TNFalpha. Science 295, 2282 2285.
3. Bernardino L., Xapelli S., Silva A. P., Jakobsen B., Poulsen F. R., Oliveira C. R., Vezzani A., Malva J. O. Zimmer J. (2005) Modulator effects of interleukin-1beta and tumor necrosis factor-alpha on AMPA-induced excitotoxicity in mouse organotypic hippocampal slice cultures. J. Neurosci. 25, 6734 6744.
4. Bigini P., Repici M., Cantarella G. et al. (2008) Recombinant human TNF-binding protein-1 (rhTBP-1) treatment delays both symptoms progression and motor neuron loss in the wobbler mouse. Neurobiol. Dis. 29, 465 476.
5. Bruce A. J., Boling W., Kindy M. S., Peschon J., Kraemer P. J., Carpenter M. K., Holtsberg F. W. Mattson M. P. (1996) Altered neuronal and microglial responses to excitotoxic and ischemic brain injury in mice lacking TNF receptors. Nat. Med. 2, 788 794.
6. Camu W. Henderson C. E. (1992) Purification of embryonic rat motoneurons by panning on a monoclonal antibody to the low-affinity NGF receptor. J. Neurosci. Methods 44, 59 70.
7. Canton T., Bohme G. A., Boireau A. et al. (2001) RPR 119990, a novel alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid antagonist: synthesis, pharmacological properties, and activity in an animal model of amyotrophic lateral sclerosis. J. Pharmacol. Exp. Ther. 299, 314 322.
8. Carlson N. G., Bacchi A., Rogers S. W. Gahring L. C. (1998) Nicotine blocks TNF-alpha-mediated neuroprotection to NMDA by an alpha-bungarotoxin- sensitive pathway. J. Neurobiol. 35, 29 36.
9. Carlson N. G., Wieggel W. A., Chen J., Bacchi A., Rogers S. W. Gahring L. C. (1999) Inflammatory cytokines IL-1 alpha, IL-1 beta, IL-6, and TNF-alpha impart neuroprotection to an excitotoxin through distinct pathways. J. Immunol. 163, 3963 3968.
10. Carriedo S. G., Yin H. Z. Weiss J. H. (1996) Motor neurons are selectively vulnerable to AMPA/kainate receptor-mediated injury in vitro. J. Neurosci. 16, 4069 4079.
11. Carriedo S. G., Sensi S. L., Yin H. Z. Weiss J. H. (2000) AMPA exposures induce mitochondrial Ca(2+) overload and ROS generation in spinal motor neurons in vitro. J. Neurosci. 20, 240 250.
12. Chadwick W., Magnus T., Martin B., Keselman A., Mattson M. P. Maudsley S. (2008) Targeting TNF-α receptors for neurotherapeutics. Trends Neurosci. 31, 504 511.
13. Chao C. C. Hu S. (1994) Tumor necrosis factor-alpha potentiates glutamate neurotoxicity in human fetal brain cell cultures. Dev. Neurosci. 16, 172 179.
14. Cheng B., Christakos S. Mattson M. P. (1994) Tumor necrosis factors protect neurons against metabolic-excitotoxic insults and promote maintenance of calcium homeostasis. Neuron 12, 139 153. (Pubitemid 24044394)
15. Couratier P., Hugon J., Sindou P., Vallat J. M. Dumas M. (1993) Cell culture evidence for neuronal degeneration in amyotrophic lateral sclerosis being linked to glutamate AMPA/kainate receptors. Lancet 341, 265 268.
16. De A., Krueger J. M. Simasko S. M. (2003) Tumor necrosis factor alpha increases cytosolic calcium responses to AMPA and KCl in primary cultures of rat hippocampal neurons. Brain Res. 981, 133 142.
17. Dolga A. M., Granic I., Blank T., Knaus H. G., Spiess J., Luiten P. G., Eisel U. L. Nijholt I. M. (2008) TNF-alpha mediates neuroprotection against glutamate-induced excitotoxicity via NF-kappaB-dependent up-regulation of K2.2 channels. J. Neurochem. 107, 1158 1167.
18. Duong F. H., Warter J. M., Poindron P. Passilly P. (1999) Effect of the nonpeptide neurotrophic compound SR 57746A on the phenotypic survival of purified mouse motoneurons. Br. J. Pharmacol. 128, 1385 1392.
19. Elliott J. L. (2001) Cytokine upregulation in a murine model of familial amyotrophic lateral sclerosis. Mol. Brain Res. 95, 172 178.
20. Ferguson A. R., Christensen R. N., Gensel J. C., Miller B. A., Sun F., Beattie E. C., Bresnahan J. C. Beattie M. S. (2008) Cell death after spinal cord injury is exacerbated by rapid TNF alpha-induced trafficking of GluR2-lacking AMPARs to the plasma membrane. J. Neurosci. 28, 11391 11400.
21. Fiers W., Beyaert R., Boone E. et al. (1995) TNF-induced intracellular signaling leading to gene induction or to cytotoxicity by necrosis or by apoptosis. J. Inflamm. 47, 67 75.
22. Fontaine V., Mohand-Said S., Hanoteau N., Fuchs C., Pfizenmaier K. Eisel U. (2002) Neurodegenerative and neuroprotective effects of tumor necrosis factor (TNF) in retinal ischemia: opposite roles of TNF receptor 1 and TNF receptor 2. J. Neurosci. 22, RC216.
23. Ghezzi P. Mennini T. (2001) Tumor necrosis factor and motoneuronal degeneration: an open problem. Neuroimmunomodulation 9, 178 182.
24. Gowing G., Dequen F., Soucy G. Julien J. P. (2006) Absence of tumor necrosis factor-alpha does not affect motor neuron disease caused by superoxide dismutase 1 mutations. J. Neurosci. 26, 11397 11402.
25. Gustin J. A., Ozes O. N., Akca H. et al. (2004) Cell type-specific expression of the IkappaB kinases determines the significance of phosphatidylinositol 3-kinase/Akt signaling to NF-kappa B activation. J. Biol. Chem. 279, 1615 1620.
26. He B. P., Wen W. Strong M. J. (2002) Activated microglia (BV-2) facilitation of TNF-alpha-mediated motor neuron death in vitro. J. Neuroimmunol. 128, 31 38.
27. Hensley K., Floyd R. A., Gordon B., Mou S., Pye Q. N., Stewart C., West M. Williamson K. (2002) Temporal patterns of cytokine and apoptosis-related gene expression in spinal cords of the G93A-SOD1 mouse model of amyotrophic lateral sclerosis. J. Neurochem. 82, 365 374.
28. 2+ permeability of KA-AMPA-gated glutamate receptor channels depends on subunit composition. Science 252, 851 853.
29. Jara J. H., Singh B. B., Floden A. M. Combs C. K. (2007) Tumor necrosis factor alpha stimulates NMDA receptor activity in mouse cortical neurons resulting in ERK-dependent death. J. Neurochem. 100, 1407 1420.
30. Leonoudakis D., Zhao P. Beattie E. C. (2008) Rapid tumor necrosis factor alpha-induced exocytosis of glutamate receptor 2-lacking AMPA receptors to extrasynaptic plasma membrane potentiates excitotoxicity. J. Neurosci. 28, 2119 2130.
31. Lobsiger C. S. Cleveland D. W. (2007) Glial cells as intrinsic components of non-cell-autonomous neurodegenerative disease. Nat. Neurosci. 10, 1355 1360.
32. Loustau V., Foltz V., Poulain C., Rozenberg S. Bruneteau G. (2009) Diagnosis of amyotrophic lateral sclerosis in a patient treated with TNFalpha blockers for ankylosing spondylitis: fortuitus association or new side effect of TNFalpha blockers? Joint Bone Spine 76, 213 214.
33. Lu W., Man H., Ju W., Trimble W. S., MacDonald J. F. Wang Y. T. (2001) Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron 29, 243 254.
34. Liu S. Q. Cull-Candy S. G. (2000) Synaptic activity at calcium permeable AMPA receptors induces a change in receptor subtype. Nature 405, 454 458.
35. Man H. Y., Wang Q., Lu W. Y. et al. (2003) Activation of PI3-kinase is required for AMPA receptor insertion during LTP of mEPSCs in cultured hippocampal neurons. Neuron 38, 611 624.
36. Marchetti L., Klein M., Schlett K., Pfizenmaier K. Eisel U. L. (2004) Tumor necrosis factor (TNF)-mediated neuroprotection against glutamate-induced excitotoxicity is enhanced by N-methyl-d-aspartate receptor activation. Essential role of a TNF receptor 2-mediated phosphatidylinositol 3-kinase-dependent NF-kappa B pathway. J. Biol. Chem. 279, 32869 32881.
37. McGeer P. L. McGeer E. G. (2002) Inflammatory processes in amyotrophic lateral sclerosis. Muscle Nerve 26, 459 470.
38. Newpher T. M. Ehlers M. D. (2008) Glutamate receptor dynamics in dendritic microdomains. Neuron 58, 472 497.
39. Nguyen M. D., Julien J. P. Rivest S. (2001) Induction of proinflammatory molecules in mice with amyotrophic lateral sclerosis: no requirement for proapoptotic interleukin-1beta in neurodegeneration. Ann. Neurol. 50, 630 639.
40. 2+ permeable alpha-amino-3-hydroxyl-5-methyl-4-isoxazole-propionate (AMPA)/kainate (Ca-A/K) channels in a subset of hippocampal pyramidal neurons. Exp. Neurol. 193, 384 393.
41. Peacey E., Miller C. C., Dunlop J. Rattray M. (2009) The four major N- and C-terminal splice variants of the excitatory amino acid transporter GLT-1 form cell surface homomeric and heteromeric assemblies. Mol. Pharmacol. 75, 1062 1073.
42. Perkinton M. S., Sihra T. S. Williams R. J. (1999) Ca(2+)-permeable AMPA receptors induce phosphorylation of cAMP response element-binding protein through a phosphatidylinositol 3-kinase-dependent stimulation of the mitogen-activated protein kinase signaling cascade in neurons. J. Neurosci. 19, 5861 5874.
43. Pezet S., Marchand F., D'Mello R., Grist J., Clark A. K., Malcangio M., Dickenson A. H., Williams R. J. McMahon S. B. (2008) Phosphatidylinositol 3-kinase is a key mediator of central sensitization in painful inflammatory conditions. J. Neurosci. 28, 4261 4270.
44. Pickering M., Cumiskey D. O'Connor J. J. (2005) Actions of TNF-alpha on glutamatergic synaptic transmission in the central nervous system. Exp. Physiol. 90, 663 670.
45. Raivich G., Liu Z. Q., Kloss C. U., Labow M., Bluethmann H. Bohatschek M. (2002) Cytotoxic potential of proinflammatory cytokines: combined deletion of TNF receptors TNFR1 and TNFR2 prevents motoneuron cell death after facial axotomy in adult mouse. Exp. Neurol. 178, 186 193.
46. Raoul C., Buhler E., Sadeghi C., Jacquier A., Aebischer P., Pettmann B., Henderson C. E. Haase G. (2006) Chronic activation in presymptomatic amyotrophic lateral sclerosis (ALS) mice of a feedback loop involving Fas, Daxx, and FasL. Proc. Natl Acad. Sci. USA 103, 6007 6012.
47. Rattray M. Bendotti C. (2006) Does excitotoxic cell death of motor neurons in ALS arise from glutamate transporter and glutamate receptor abnormalities? Exp. Neurol. 201, 15 23.
48. Robertson J., Beaulieu J. M., Doroudchi M. M., Durham H. D., Julien J. P. Mushynski W. E. (2001) Apoptotic death of neurons exhibiting peripherin aggregates is mediated by the proinflammatory cytokine tumor necrosis factor-alpha. J. Cell Biol. 155, 217 226.
49. Roy J., Minotti S., Dong L., Figlewicz D. A. Durham H. D. (1998) Glutamate potentiates the toxicity of mutant Cu/Zn-superoxide dismutase in motor neurons by postsynaptic calcium-dependent mechanisms. J. Neurosci. 18, 9673 9684.
50. Sanna P. P., Cammalleri M., Berton F., Simpson C., Lutjens R., Bloom F. E. Francesconi W. (2002) Phosphatidylinositol 3-kinase is required for the expression but not for the induction or the maintenance of long-term potentiation in the hippocampal CA1 region. J. Neurosci. 22, 3359 3365.
51. Schroeter H., Bahia P., Spencer J. P., Sheppard O., Rattray M., Cadenas E., Rice-Evans C. Williams R. J. (2007) (-)Epicatechin stimulates ERK-dependent cyclic AMP response element activity and upregulates GluR2 in cortical neurons. J. Neurochem. 101, 1596 1606.
52. Sedel F., Béchade C., Vyas S. Triller A. (2004) Macrophage-derived tumor necrosis factor alpha, an early developmental signal for motoneuron death. J. Neurosci. 24, 2236 2246.
53. Stellwagen D. Malenka R. C. (2006) Synaptic scaling mediated by glial TNF-alpha. Nature 440, 1054 1059.
54. Stellwagen D., Beattie E. C., Seo J. Y. Malenka R. C. (2005) Differential regulation of AMPA receptor and GABA receptor trafficking by tumor necrosis factor-alpha. J. Neurosci. 25, 3219 3228.
55. Stommel E. W., van Hoff R. M., Graber D. J., Bercury K. K., Langford G. M. Harris B. T. (2007) Tumor necrosis factor-alpha induces changes in mitochondrial cellular distribution in motor neurons. Neuroscience 146, 1013 1019.
56. Tartaglia L. A., Rothe M., Hu Y. F. Goeddel D. V. (1993) Tumor necrosis factor's cytotoxic activity is signaled by the p55 TNF receptor. Cell 73, 213 216.
57. Tateno M., Sadakata H., Tanaka M. et al. (2004) Calcium permeable AMPA receptors promote misfolding of mutant SOD1 protein and development of amyotrophic lateral sclerosis in a transgenic mouse model. Hum. Mol. Genet. 13, 2183 2196.
58. Terrado J., Monnier D., Perrelet D. et al. (2000) Soluble TNF receptors partially protect injured motoneurons in the postnatal CNS. Eur. J. Neurosci. 12, 3443 3447.
59. Tortarolo M., Crossthwaite A. J., Conforti L., Spencer J. P., Williams R. J., Bendotti C. Rattray M. (2004) Expression of SOD1 G93A or wild-type SOD1 in primary cultures of astrocytes down-regulates the glutamate transporter GLT-1: lack of involvement of oxidative stress. J. Neurochem. 88, 481 493.
60. Van Damme P., Van Den Bosch L., Van Houtte E., Callewaert G. Robberecht W. (2002) GluR2-dependent properties of AMPA receptors determine the selective vulnerability of motor neurons to excitotoxicity. J. Neurophysiol. 88, 1279 1287.
61. Van Damme P., Leyssen M., Callewaert G., Robberecht W. Van Den Bosch L. (2003) The AMPA receptor antagonist NBQX prolongs survival in a transgenic mouse model of amyotrophic lateral sclerosis. Neurosci. Lett. 343, 81 84.
62. Vandenberghe W., Robberecht W. Brorson J. R. (2000) AMPA receptor calcium permeability, GluR2 expression, and selective motoneuron vulnerability. J. Neurosci. 20, 123 132.
63. Veglianese P., Lo Coco D., Bao Cutrona M. et al. (2006) Activation of the p38MAPK cascade is associated with upregulation of TNF alpha receptors in the spinal motor neurons of mouse models of familial ALS. Mol. Cell. Neurosci. 31, 218 231.
64. Wen W., Sanelli T., Ge W., Strong W. Strong M. J. (2006) Activated microglial supernatant induced motor neuron cytotoxicity is associated with upregulation of the TNFR1 receptor. Neurosci. Res. 55, 87 95.
65. Williams R. J. Glowinski J. (1996) Cyclothiazide unmasks an AMPA-evoked release of arachidonic acid from cultured striatal neurones. J. Neurochem. 67, 1551 1558.
66. Yang L., Lindholm K., Konishi Y., Li R. Shen Y. (2002) Target depletion of distinct tumor necrosis factor receptor subtypes reveals hippocampal neuron death and survival through different signal transduction pathways. J. Neurosci. 22, 3025 3032.
67. Yoshihara T., Ishigaki S., Yamamoto M., Liang Y., Niwa J., Takeuchi H., Doyu M. Sobue G. (2002) Differential expression of inflammation- and apoptosis-related genes in spinal cords of a mutant SOD1 transgenic mouse model of familial amyotrophic lateral sclerosis. J. Neurochem. 80, 158 167.
68. Yu Z., Cheng G., Wen X., Wu G. D., Lee W. T. Pleasure D. (2002) Tumor necrosis factor alpha increases neuronal vulnerability to excitotoxic necrosis by inducing expression of the AMPA-glutamate receptor subunit GluR1 via an acid sphingomyelinase- and NF-kappaB-dependent mechanism. Neurobiol. Dis. 11, 199 213.
69. Yuasa T., Ohno S., Kehrl J. H. Kyriakis J. M. (1998) Tumor necrosis factor signaling to stress-activated protein kinase (SAPK)/Jun NH2-terminal kinase (JNK) and p38. Germinal center kinase couples TRAF2 to mitogen-activated protein kinase/ERK kinase kinase 1 and SAPK while receptor interacting protein associates with a mitogen-activated protein kinase kinase kinase upstream of MKK6 and p38. J. Biol. Chem. 273, 22681 22692.