The AMPA receptor subunits GluR-A and GluR-B reciprocally modulate spinal synaptic plasticity and inflammatory pain

Neuron

Volumn 44, Issue 4, 2004, Pages 637-650

  Hartmann, Bettina ^a   Ahmadi, Seifollah ^b   Heppenstall, Paul A ^c,d   Lewin, Gary R ^d   Schott, Claus ^a   Borchardt, Thilo ^e   Seeburg, Peter H ^e   Zeilhofer, Hanns Ulrich ^b   Sprengel, Rolf ^e   Kuner, Rohini ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^e MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; CALCIUM CHANNEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; HYPERALGESIA; MOUSE; NERVE CELL PLASTICITY; NOCICEPTION; NONHUMAN; PAIN; PRIORITY JOURNAL; RECEPTOR BINDING;

ANIMALS; BRAIN; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; MICE; MICE, KNOCKOUT; NEURAL PATHWAYS; NEURONAL PLASTICITY; NOCICEPTORS; ORGAN CULTURE TECHNIQUES; PAIN; RECEPTORS, AMPA; SPINAL CORD;

EID: 8844234340     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2004.10.029     Document Type: Article

References (58)

1. 2 selectively blocks inhibitory glycinergic neurotransmission onto rat superficial dorsal horn neurons. Nat. Neurosci. 5:2002;34-40
2. Albuquerque C., Lee C.J., Jackson A.C., MacDermott A.B. Subpopulations of GABAergic and non-GABAergic rat dorsal horn neurons express Ca2+-permeable AMPA receptors. Eur. J. Neurosci. 11:1999;2758-2766
3. Borchardt, T. (2002). Die Konstruktion von Mäusen mit veränderten AMPA-Rezeptoren. Dissertation, University of Heidelberg, Germany.
4. Brown K.M., Wrathall J.R., Yasuda R.P., Wolfe B.B. Quantitative measurement of glutamate receptor subunit protein expression in the postnatal rat spinal cord. Brain Res. Dev. Brain Res. 137:2002;127-133
5. Burnashev N., Monyer H., Seeburg P.H., Sakmann B. Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit. Neuron. 8:1992;189-198
6. Cirino G., Peers S.H., Wallace J.L., Flower R.J. A study of phospholipase A2-induced oedema in rat paw. Eur. J. Pharmacol. 166:1989;505-510
7. Davies J., Watkins J.C. Role of excitatory amino acid receptors in mono- and polysynaptic excitation in the cat spinal cord. Exp. Brain Res. 49:1983;280-290
8. Dodt H.U., Zieglgänsberger W. Infrared videomicroscopy. a new look at neuronal structure and function Trends Neurosci. 17:1994;453-458
9. Engelman H.S., MacDermott A.B. Presynaptic ionotropic receptors and control of transmitter release. Nat. Rev. Neurosci. 5:2004;135-145
10. Engelman H.S., Allen T.B., MacDermott A.B. The distribution of neurons expressing calcium-permeable AMPA receptors in the superficial laminae of the spinal cord dorsal horn. J. Neurosci. 19:1999;2081-2089
11. Fang L., Wu J., Lin Q., Willis W.D. Protein kinases regulate the phosphorylation of the GluR1 subunit of AMPA receptors of spinal cord in rats following noxious stimulation. Brain Res. Mol. Brain Res. 118:2003;160-165. a
12. Fang L., Wu J., Zhang X., Lin Q., Willis W.D. Increased phosphorylation of the GluR1 subunit of spinal cord alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionate receptor in rats following intradermal injection of capsaicin. Neuroscience. 122:2003;237-245. b
13. Flor H. The functional organization of the brain in chronic pain. Prog. Brain Res. 129:2000;313-322
14. Flor H. Painful memories. Can we train chronic pain patients to 'forget' their pain? EMBO Rep. 3:2002;288-291
15. Gebhart G.F. Descending modulation of pain. Neurosci. Biobehav. Rev. 27:2004;729-737
16. Geiger J.R., Melcher T., Koh D.S., Sakmann B., Seeburg P.H., Jonas P., Monyer H. Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron. 15:1995;193-204
17. Gu J.G., Albuquerque C., Lee C.J., MacDermott A.B. Synaptic strengthening through activation of Ca2+-permeable AMPA receptors. Nature. 381:1996;793-796
18. Hargreaves K.M., Dubner F., Brown F., Flores C., Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain. 32:1988;77-88
19. Heppenstall P.A., Lewin G.R. BDNF but not NT-4 is required for normal flexion reflex plasticity and function. Proc. Natl. Acad. Sci. USA. 98:2001;8107-8112
20. Ikeda H., Heinke B., Ruscheweyh R., Sandkuhler J. Synaptic plasticity in spinal lamina I projection neurons that mediate hyperalgesia. Science. 299:2003;1237-1240
21. Ji R.R., Baba H., Brenner G.J., Woolf C.J. Nociceptive-specific activation of ERK in spinal neurons contributes to pain hypersensitivity. Nat. Neurosci. 2:1999;1114-1119
22. Ji R.R., Befort K., Brenner G.J., Woolf C.J. ERK MAP kinase activation in superficial spinal cord neurons induces prodynorphin and NK-1 upregulation and contributes to persistent inflammatory pain hypersensitivity. J. Neurosci. 22:2002;478-485
23. Jia Z., Agopyan N., Miu P., Xiong Z., Henderson J., Gerlai R., Taverna F.A., Velumian A., MacDonald J., Carlen P., et al. Enhanced LTP in mice deficient in the AMPA receptor GluR2. Neuron. 17:1996;945-956
24. Johansen J.P., Fields H.L., Manning B.H. The affective component of pain in rodents. direct evidence for a contribution of the anterior cingulate cortex Proc. Natl. Acad. Sci. USA. 98:2001;8077-8082
25. Ju W., Morishita W., Tsui J., Gaietta G., Deerinck T.J., Adams S.R., Garner C.C., Tsien R.Y., Ellisman M.H., Malenka R.C. Activity-dependent regulation of dendritic synthesis and trafficking of AMPA receptors. Nat. Neurosci. 7:2004;244-253
26. Kawahara Y., Ito K., Sun H., Aizawa H., Kanazawa I., Kwak S. Glutamate receptors. RNA editing and death of motor neurons Nature. 427:2004;801
27. Kolhekar R., Meller S.T., Gebhart G.F. Characterisation of the role of spinal NMDA receptors in thermal nociception in the rat. Neuroscience. 57:1993;385-395
28. Kolhekar R., Murphy S., Gebhart G.F. Thalamic NMDA receptors modulate inflammation-produced hyperalgesia in the rat. Pain. 71:1997;31-40
29. Laird J.M.A., Roza C., De Felipe C., Hunt S.P., Cervero F. Role of central and peripheral tachykinin NK1 receptors in capsaicin-induced pain and hyperalgesia in mice. Pain. 90:2001;97-103
30. Lee C.J., Bardoni R., Tong C.K., Engelman H.S., Joseph D.J., Magherini P.C., MacDermott A.B. Functional expression of AMPA receptors on central terminals of rat dorsal root ganglion neurons and presynaptic inhibition of glutamate release. Neuron. 35:2002;135-146
31. Lee H.K., Takamiya K., Han J.S., Man H., Kim C.H., Rumbaugh G., Yu S., Ding L., He C., Petralia R.S., et al. Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory. Cell. 112:2003;631-643
32. Li J., Simone D.A., Larson A.A. Windup leads to characteristics of central sensitization. Pain. 79:1999;75-82
33. Liu S.-Q.J., Cull-Candy S. Synaptic activity at calcium-permeable AMPA receptors induces a switch in receptor subtype. Nature. 405:2000;454-458
34. Lu C.R., Hwang S.J., Phend K.D., Rustioni A., Valtschanoff J.G. Primary afferent terminals in spinal cord express presynaptic AMPA receptors. J. Neurosci. 22:2002;9522-9529
35. Ma Q.P., Woolf C.J. Basal and touch-evoked fos-like immunoreactivity during experimental inflammation in the rat. Pain. 67:1996;307-316
36. Malinow R., Malenka R.C. AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25:2002;103-126
37. Monyer H., Seeburg P.H., Wisden W. Glutamate-operated channels. developmentally early and mature forms arise by alternative splicing Neuron. 6:1991;799-810
38. Nagy J.I., Hunt S.P. Fluoride-resistant acid phosphatase-containing neurones in dorsal root ganglia are separate from those containing substance P or somatostatin. Neuroscience. 7:1982;89-97
39. Nagy G.G., Al-Ayyan M., Andrew D., Fukaya M., Watanabe M., Todd A.J. Widespread expression of the AMPA receptor GluR2 subunit at glutamatergic synapses in the rat spinal cord and phosphorylation of GluR1 in response to noxious stimulation revealed with an antigen-unmasking method. J. Neurosci. 24:2004;5766-5777
40. 2+-impermeable AMPA receptors among populations of neurons. J. Comp. Neurol. 385:1997;456-476
41. Reisel D., Bannerman D.M., Schmitt W.B., Deacon R.M., Flint J., Borchardt T., Seeburg P.H., Rawlins J.N. Spatial memory dissociations in mice lacking GluR1. Nat. Neurosci. 5:2002;868-873
42. Sandkühler J. Learning and memory in pain pathways. Pain. 88:2000;113-118
43. Sandkühler J. Fear the pain. Lancet. 360:2002;426
44. Seeburg, P.H., Single, F., Kuner, T., Higuchi, M., and Sprengel, R. (2001). Genetic manipulation of key determinants of ion flow in glutamate receptor channels in the mouse. Brain Res. 13, 907, 233-243.
45. Shi S., Hayashi Y., Esteban J.A., Malinow R. Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell. 105:2001;331-343
46. Sutton M.A., Schmidt E.F., Choi K.H., Schad C.A., Whisler K., Simmons D., Karanian D.A., Monteggia L.M., Neve R.L., Self D.W. Extinction-induced upregulation in AMPA receptors reduces cocaine-seeking behaviour. Nature. 421:2003;70-75
47. Takahashi T., Svoboda K., Malinow R. Experience strengthening transmission by driving AMPA receptors into synapses. Science. 299:2003;1585-1588
48. Thomas G.M., Huganir R.L. MAPK cascade signalling and synaptic plasticity. Nat. Rev. Neurosci. 5:2004;173-183
49. Thomas M.J., Beurrier C., Bonci A., Malenka R.C. Long-term depression in the nucleus accumbens. a neural correlate of behavioral sensitization to cocaine Nat. Neurosci. 4:2001;1217-1223
50. Tinazzi M., Fiaschi A., Rosso T., Faccioli F., Grosslercher J., Aglioti S.M. Neuroplastic changes related to pain occur at multiple levels of the human somatosensory system. A somatosensory-evoked potentials study in patients with cervical radicular pain J. Neurosci. 20:2000;9277-9283
51. Tjolsen A., Berge O.G., Hunskaar S., Rosland J.H., Hole K. The formalin test. an evaluation of the method Pain. 51:1992;5-17
52. Tolle T.R., Berthele A., Zieglgänsberger W., Seeburg P.H., Wisden W. The differential expression of 16 NMDA and non-NMDA receptor subunits in the rat spinal cord and in periaqueductal gray. J. Neurosci. 13:1993;5009-5028
53. Vaccarino A.L., Melzack R. Temporal processes of formalin pain. differential role of the cingulum bundle, fornix pathway and medial bulboreticular formation Pain. 49:1992;257-271
54. Wilding T.J., Huettner J.E. Differential antagonism of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid-preferring and kainate-preferring receptors by 2,3-benzodiazepines. Mol. Pharmacol. 47:1995;582-587
55. Willis, W.D., Jr. (1997). Is central sensitization of nociceptive transmission in the spinal cord a variety of long-term potentiation? Neuroreport. 8, iii.
56. Woolf C.J., Salter M.W. Neuronal plasticity. increasing the gain in pain Science. 288:2000;1765-1769
57. Zamanillo D., Sprengel R., Hvalby O., Jensen V., Burnashev N., Rozov A., Kaiser K.M., Koster H.J., Borchardt T., Worley P., et al. Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science. 284:1999;1805-1811
58. Zhou Q.Q., Imbe H., Zou S., Dubner R., Ren K. Selective upregulation of the flip-flop splice variants of AMPA receptor subunits in the rat spinal cord after hindpaw inflammation. Brain Res. Mol. Brain Res. 88:2001;186-193