G protein-coupled receptor kinase 2 and group i metabotropic glutamate receptors mediate inflammation-induced sensitization to excitotoxic neurodegeneration

Annals of Neurology

Volumn 73, Issue 5, 2013, Pages 667-678

  Degos, Vincent ^a,b,c,d   Peineau, Stéphane ^a,b,c,e   Nijboer, Cora ^f   Kaindl, Angela M ^a,b,c,r   Sigaut, Stéphanie ^a,b,c   Favrais, Géraldine ^a,b,c   Plaisant, Frank ^a,b,c   Teissier, Natacha ^a,b,c   Gouadon, Elodie ^g,h,i   Lombet, Alain ^g,i   Saliba, Elie ^j   Collingridge, Graham L ^e,k,l   Maze, Mervyn ^d   Nicoletti, Ferdinando ^m,n   Heijnen, Cobi ^f   Mantz, Jean ^a,b,c,o   Kavelaars, Annemieke ^f,p   Gressens, Pierre ^a,b,c,q  

^a HÔPITAL ROBERT DEBRÉ   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c PremUP   (France)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF BRISTOL   (United Kingdom)

^f UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^g INSERM   (France)

^h CENTRE CHIRURGICAL MARIE LANNELONGUE   (France)

ⁱ UNIVERSITÉ PARIS SACLAY   (France)

^j UNIVERSITÉ DE TOURS   (France)

^k UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^l Seoul National University   (South Korea)

^m SAPIENZA UNIVERSITY OF ROME   (Italy)

ⁿ IRCCS NEUROMED   (Italy)

^o BEAUJON HOSPITAL   (France)

^p UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^q KING'S COLLEGE LONDON   (United Kingdom)

^r Universitätsmedizin   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED RECEPTOR KINASE 2; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; METABOTROPIC RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXCITOTOXICITY; GENE DELETION; HUMAN; IN VIVO STUDY; MOUSE; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; SENSITIZATION;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; CALCIUM; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CEREBRAL CORTEX; CYTOKINES; DISEASE MODELS, ANIMAL; EXCITATORY AMINO ACID AGONISTS; FEMALE; G-PROTEIN-COUPLED RECEPTOR KINASE 2; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMANS; IBOTENIC ACID; INFLAMMATION; INTERLEUKIN-1BETA; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURODEGENERATIVE DISEASES; NEURONS; NEUROTOXICITY SYNDROMES; PHOSPHOLIPASE C BETA; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RECEPTORS, METABOTROPIC GLUTAMATE;

EID: 84878321437     PISSN: 03645134     EISSN: 15318249     Source Type: Journal    
DOI: 10.1002/ana.23868     Document Type: Article

References (53)

1. Lipton SA, Rosenberg PA. Excitatory amino acids as a final common pathway for neurologic disorders. N Engl J Med 1994;330:613-622.
2. Lipton SA. Pathologically activated therapeutics for neuroprotection. Nat Rev Neurosci 2007;8:803-808.
3. Degos V, Favrais G, Kaindl AM, et al. Inflammation processes in perinatal brain damage. J Neural Transm 2010;117:1009-1017.
4. Dommergues MA, Patkai J, Renauld JC, et al. Proinflammatory cytokines and interleukin-9 exacerbate excitotoxic lesions of the newborn murine neopallium. Ann Neurol 2000;47:54-63.
5. McColl BW, Allan SM, Rothwell NJ. Systemic infection, inflammation and acute ischemic stroke. Neuroscience 2009;158:1049-1061.
6. Smith CJ, Emsley HC, Gavin CM, et al. Peak plasma interleukin-6 and other peripheral markers of inflammation in the first week of ischaemic stroke correlate with brain infarct volume, stroke severity and long-term outcome. BMC Neurol 2004;4:2.
7. Aden U, Favrais G, Plaisant F, et al. Systemic inflammation sensitizes the neonatal brain to excitotoxicity through a pro-/antiinflammatory imbalance: key role of TNFalpha pathway and protection by etanercept. Brain Behav Immun 2010;24:747-758.
8. Dale LB, Bhattacharya M, Anborgh PH, et al. G protein-coupled receptor kinase-mediated desensitization of metabotropic glutamate receptor 1A protects against cell death. J Biol Chem 2000;275:38213-38220.
9. Reiter E, Lefkowitz RJ. GRKs and beta-arrestins: roles in receptor silencing, trafficking and signaling. Trends Endocrinol Metab 2006;17:159-165.
10. Alves-Filho JC, Sonego F, Souto FO, et al. Interleukin-33 attenuates sepsis by enhancing neutrophil influx to the site of infection. Nat Med 2010;16:708-712.
11. Marret S, Mukendi R, Gadisseux JF, et al. Effect of ibotenate on brain development: an excitotoxic mouse model of microgyria and posthypoxic-like lesions. J Neuropathol Exp Neurol 1995;54:358-370.
12. Rousset CI, Kassem J, Olivier P, et al. Antenatal bacterial endotoxin sensitizes the immature rat brain to postnatal excitotoxic injury. J Neuropathol Exp Neurol 2008;67:994-1000.
13. Favrais G, Schwendimann L, Gressens P, Lelievre V. Cyclooxygenase- 2 mediates the sensitizing effects of systemic IL-1-beta on excitotoxic brain lesions in newborn mice. Neurobiol Dis 2007;25:496-505.
14. Wang X, Stridh L, Li W, et al. Lipopolysaccharide sensitizes neonatal hypoxic-ischemic brain injury in a MyD88-dependent manner. J Immunol 2009;183:7471-7477.
15. Dantzer R, OConnor JC, Freund GG, et al. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci 2008;9:46-56.
16. Ribeiro FM, Ferreira LT, Paquet M, et al. Phosphorylation-independent regulation of metabotropic glutamate receptor 5 desensitization and internalization by G protein-coupled receptor kinase 2 in neurons. J Biol Chem 2009;284:23444-23453.
17. Nijboer CH, Kavelaars A, Vroon A, et al. Low endogenous G-protein- coupled receptor kinase 2 sensitizes the immature brain to hypoxia-ischemia- induced gray and white matter damage. J Neurosci 2008;28:3324-3332.
18. Nijboer CH, Heijnen CJ, Willemen HL, et al. Cell-specific roles of GRK2 in onset and severity of hypoxic-ischemic brain damage in neonatal mice. Brain Behav Immun 2010;24:420-426.
19. McColl BW, Rothwell NJ, Allan SM. Systemic inflammatory stimulus potentiates the acute phase and CXC chemokine responses to experimental stroke and exacerbates brain damage via interleukin- 1- and neutrophil-dependent mechanisms. J Neurosci 2007;27:4403-4412.
20. Eklind S, Mallard C, Leverin AL, et al. Bacterial endotoxin sensitizes the immature brain to hypoxic-ischaemic injury. Eur J Neurosci 2001;13:1101-1106.
21. Parry-Jones AR, Liimatainen T, Kauppinen RA, et al. Interleukin-1 exacerbates focal cerebral ischemia and reduces ischemic brain temperature in the rat. Magn Reson Med 2008;59:1239-1249.
22. Holmes C, Cunningham C, Zotova E, et al. Systemic inflammation and disease progression in Alzheimer disease. Neurology 2009;73:768-774.
23. Moreno B, Jukes JP, Vergara-Irigaray N, et al. Systemic inflammation induces axon injury during brain inflammation. Ann Neurol 2011;70:932-942.
24. Nicoletti F, Bruno V, Catania MV, et al. Group-I metabotropic glutamate receptors: hypotheses to explain their dual role in neurotoxicity and neuroprotection. Neuropharmacology 1999;38:1477-1484.
25. Caraci F, Battaglia G, Sortino MA, et al. Metabotropic glutamate receptors in neurodegeneration/neuroprotection: still a hot topic? Neurochem Int 2012;61:559-565.
26. Pisani A, Gubellini P, Bonsi P, et al. Metabotropic glutamate receptor 5 mediates the potentiation of N-methyl-D-aspartate responses in medium spiny striatal neurons. Neuroscience 2001;106:579-587.
27. Xu W, Wong TP, Chery N, et al. Calpain-mediated mGluR1alpha truncation: a key step in excitotoxicity. Neuron 2007;53:399-412.
28. Alagarsamy S, Saugstad J, Warren L, et al. NMDA-induced potentiation of mGluR5 is mediated by activation of protein phosphatase 2B/calcineurin. Neuropharmacology 2005;49(suppl 1):135-145.
29. Brakeman PR, Lanahan AA, OBrien R, et al. Homer: a protein that selectively binds metabotropic glutamate receptors. Nature 1997;386:284-288.
30. Kato A, Ozawa F, Saitoh Y, et al. Novel members of the Vesl/ Homer family of PDZ proteins that bind metabotropic glutamate receptors. J Biol Chem 1998;273:23969-23975.
31. Xiao B, Tu JC, Petralia RS, et al. Homer regulates the association of group 1 metabotropic glutamate receptors with multivalent complexes of homer-related, synaptic proteins. Neuron 1998;21:707-716.
32. Tu JC, Xiao B, Naisbitt S, et al. Coupling of mGluR/Homer and PSD-95 complexes by the Shank family of postsynaptic density proteins. Neuron 1999;23:583-592.
33. Doherty AJ, Palmer MJ, Henley JM, et al. (RS)22-chloro-5- hydroxyphenylglycine (CHPG) activates mGlu5, but no mGlu1, receptors expressed in CHO cells and potentiates NMDA responses in the hippocampus. Neuropharmacology 1997;36:265-267.
34. Awad H, Hubert GW, Smith Y, et al. Activation of metabotropic glutamate receptor 5 has direct excitatory effects and potentiates NMDA receptor currents in neurons of the subthalamic nucleus. J Neurosci 2000;20:7871-7879.
35. Collett VJ, Collingridge GL. Interactions between NMDA receptors and mGlu5 receptors expressed in HEK293 cells. Br J Pharmacol 2004;142:991-1001.
36. Bruno V, Copani A, Knopfel T, et al. Activation of metabotropic glutamate receptors coupled to inositol phospholipid hydrolysis amplifies NMDA-induced neuronal degeneration in cultured cortical cells. Neuropharmacology 1995;34:1089-1098.
37. Ugolini A, Corsi M, Bordi F. Potentiation of NMDA and AMPA responses by the specific mGluR5 agonist CHPG in spinal cord motoneurons. Neuropharmacology 1999;38:1569-1576.
38. Nijboer CH, van der Kooij MA, van Bel F, et al. Inhibition of the JNK/AP-1 pathway reduces neuronal death and improves behavioral outcome after neonatal hypoxic-ischemic brain injury. Brain Behav Immun 2010;24:812-821.
39. Nicolas CS, Peineau S, Amici M, et al. The Jak/STAT pathway is involved in synaptic plasticity. Neuron 2012;73:374-390.
40. Brochu ME, Girard S, Lavoie K, Sebire G. Developmental regulation of the neuroinflammatory responses to LPS and/or hypoxia-ischemia between preterm and term neonates: an experimental study. J Neuroinflammation 2011;8:55.
41. McClain CJ, Cohen D, Ott L, et al. Ventricular fluid interleukin-1 activity in patients with head injury. J Lab Clin Med 1987;110:48-54.
42. Serrats J, Schiltz JC, Garcia-Bueno B, et al. Dual roles for perivascular macrophages in immune-to-brain signaling. Neuron 2010;65:94-106.
43. Gardoni F, Boraso M, Zianni E, et al. Distribution of interleukin-1 receptor complex at the synaptic membrane driven by interleukin- 1beta and NMDA stimulation. J Neuroinflammation 2011;8:14.
44. Allan SM, Tyrrell PJ, Rothwell NJ. Interleukin-1 and neuronal injury. Nat Rev Immunol 2005;5:629-640.
45. Beattie EC, Stellwagen D, Morishita W, et al. Control of synaptic strength by glial TNFalpha. Science 2002;295:2282-2285.
46. Raivich G, Bohatschek M, Kloss CU, et al. Neuroglial activation repertoire in the injured brain: graded response, molecular mechanisms and cues to physiological function. Brain Res Brain Res Rev 1999;30:77-105.
47. Hedtjarn M, Leverin AL, Eriksson K, et al. Interleukin-18 involvement in hypoxic-ischemic brain injury. J Neurosci 2002;22:5910-5919.
48. Mirabelli-Badenier M, Braunersreuther V, Viviani GL, et al. CC and CXC chemokines are pivotal mediators of cerebral injury in ischaemic stroke. Thromb Haemost 2011;105:409-420.
49. Bednarek N, Clement Y, Lelievre V, et al. Ontogeny of MMPs and TIMPs in the murine neocortex. Pediatr Res 2009;65:296-300.
50. Doumazane E, Scholler P, Zwier JM, et al. A new approach to analyze cell surface protein complexes reveals specific heterodimeric metabotropic glutamate receptors. FASEB J 2011;25:66-77
51. Kniazeff J, Bessis AS, Maurel D, et al. Closed state of both binding domains of homodimeric mGlu receptors is required for full activity. Nat Struct Mol Biol 2004;11:706-713.
52. DAntoni S, Berretta A, Seminara G, et al. A prolonged pharmacological blockade of type-5 metabotropic glutamate receptors protects cultured spinal cord motor neurons against excitotoxic death. Neurobiol Dis 2011;42:252-264.
53. Nicoletti F, Bockaert J, Collingridge GL, et al. Metabotropic glutamate receptors: from the workbench to the bedside. Neuropharmacology 2011;60:1017-1041.