Peripheral nerve injury produces a sustained shift in the balance between glutamate release and uptake in the dorsal horn of the spinal cord

Pain

Volumn 153, Issue 12, 2012, Pages 2422-2431

  Inquimbert, Perrine ^a,b   Bartels, Karsten ^c,d   Babaniyi, Olusegun B ^a   Barrett, Lee B ^a   Tegeder, Irmgard ^e   Scholz, Joachim ^c,f  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b INSTITUT DE PHARMACOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

^e GOETHE UNIVERSITY   (Germany)

^f College of Physicians and Surgeons ^*  (United States)

Author keywords

Glutamate release; Glutamate uptake; mGluR5; Neuropathic pain; Spinal dorsal horn

Indexed keywords

CEFTRIAXONE; GLUTAMIC ACID; VESICULAR GLUTAMATE TRANSPORTER 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CEREBROSPINAL FLUID; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; EXPRESSION VECTOR; LAMINA PROPRIA; MALE; NERVE CELL; NEUROPATHIC PAIN; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; RAT; SPARED NERVE INJURY; SPINAL CORD DORSAL HORN;

ANIMALS; CHRONIC PAIN; GLUTAMIC ACID; MALE; NEURALGIA; NEUROTRANSMITTER AGENTS; PERIPHERAL NERVE INJURIES; POSTERIOR HORN CELLS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84868544240     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2012.08.011     Document Type: Article

References (66)

1. F. Amaya, T.A. Samad, L. Barrett, D.C. Broom, and C.J. Woolf Periganglionic inflammation elicits a distally radiating pain hypersensitivity by promoting COX-2 induction in the dorsal root ganglion PAIN® 142 2009 59 67
2. J.J. Azkue, X.G. Liu, M. Zimmermann, and J. Sandkühler Induction of long-term potentiation of C fibre-evoked spinal field potentials requires recruitment of group I, but not group II/III metabotropic glutamate receptors PAIN® 106 2003 373 379
3. A.L. Bailey, and A. Ribeiro-da-Silva Transient loss of terminals from non-peptidergic nociceptive fibers in the substantia gelatinosa of spinal cord following chronic constriction injury of the sciatic nerve Neuroscience 138 2006 675 690
4. R. Bardoni, C. Torsney, C.K. Tong, M. Prandini, and A.B. MacDermott Presynaptic NMDA receptors modulate glutamate release from primary sensory neurons in rat spinal cord dorsal horn J Neurosci 24 2004 2774 2781
5. A.I. Basbaum, D.M. Bautista, G. Scherrer, and D. Julius Cellular and molecular mechanisms of pain Cell 139 2009 267 284
6. U.V. Berger, T.M. DeSilva, W. Chen, and P.A. Rosenberg Cellular and subcellular mRNA localization of glutamate transporter isoforms GLT1a and GLT1b in rat brain by in situ hybridization J Comp Neurol 492 2005 78 89
7. G. Bhave, F. Karim, S.M. Carlton, and R.W. Gereau Peripheral group I metabotropic glutamate receptors modulate nociception in mice Nat Neurosci 4 2001 417 423
8. B.C. Binns, Y. Huang, V.M. Goettl, K.V. Hackshaw, and R.L. Stephens Jr. Glutamate uptake is attenuated in spinal deep dorsal and ventral horn in the rat spinal nerve ligation model Brain Res 1041 2005 38 47
9. S.M. Carlton, and G.L. Hargett Colocalization of metabotropic glutamate receptors in rat dorsal root ganglion cells J Comp Neurol 501 2007 780 789
10. W. Chen, V. Mahadomrongkul, U.V. Berger, M. Bassan, T. DeSilva, K. Tanaka, N. Irwin, C. Aoki, and P.A. Rosenberg The glutamate transporter GLT1a is expressed in excitatory axon terminals of mature hippocampal neurons J Neurosci 24 2004 1136 1148
11. W. Chen, G. Zhang, and J.C. Marvizon NMDA receptors in primary afferents require phosphorylation by Src family kinases to induce substance P release in the rat spinal cord Neuroscience 166 2010 924 934
12. N.C. Danbolt Glutamate uptake Prog Neurobiol 65 2001 1 105
13. I. Decosterd, and C.J. Woolf Spared nerve injury: an animal model of persistent peripheral neuropathic pain PAIN® 87 2000 149 158
14. D. Derjean, S. Bertrand, G. Le Masson, M. Landry, V. Morisset, and F. Nagy Dynamic balance of metabotropic inputs causes dorsal horn neurons to switch functional states Nat Neurosci 6 2003 274 281
15. H.S. Engelman, R.L. Anderson, C. Daniele, and A.B. Macdermott Presynaptic alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors modulate release of inhibitory amino acids in rat spinal cord dorsal horn Neuroscience 139 2006 539 553
16. M. Ghosh, Y. Yang, J.D. Rothstein, and M.B. Robinson Nuclear factor-kappaB contributes to neuron-dependent induction of glutamate transporter-1 expression in astrocytes J Neurosci 31 2011 9159 9169
17. B. Heinke, and J. Sandkühler Group I metabotropic glutamate receptor-induced Ca(2+)-gradients in rat superficial spinal dorsal horn neurons Neuropharmacology 52 2007 1015 1023
18. S. Holmseth, H.A. Scott, K. Real, K.P. Lehre, T.B. Leergaard, J.G. Bjaalie, and N.C. Danbolt The concentrations and distributions of three C-terminal variants of the GLT1 (EAAT2; slc1a2) glutamate transporter protein in rat brain tissue suggest differential regulation Neuroscience 162 2009 1055 1071
19. H.J. Hu, G. Bhave, and R.W. Gereau Prostaglandin and protein kinase A-dependent modulation of vanilloid receptor function by metabotropic glutamate receptor 5: potential mechanism for thermal hyperalgesia J Neurosci 22 2002 7444 7452
20. H.J. Hu, and R.W. Gereau Metabotropic glutamate receptor 5 regulates excitability and Kv4.2-containing K channels primarily in excitatory neurons of the spinal dorsal horn J Neurophysiol 105 2011 3010 3021
21. Y. Hu, W. Li, L. Lu, J. Cai, X. Xian, M. Zhang, Q. Li, and L. Li An anti-nociceptive role for ceftriaxone in chronic neuropathic pain in rats PAIN® 148 2010 284 301
22. L.J. Hudson, S. Bevan, K. McNair, C. Gentry, A. Fox, R. Kuhn, and J. Winter Metabotropic glutamate receptor 5 upregulation in A-fibers after spinal nerve injury: 2-methyl-6-(phenylethynyl)-pyridine (MPEP) reverses the induced thermal hyperalgesia J Neurosci 22 2002 2660 2668
23. H. Jia, A. Rustioni, and J.G. Valtschanoff Metabotropic glutamate receptors in superficial laminae of the rat dorsal horn J Comp Neurol 410 1999 627 642
24. G.A. Kerchner, G.D. Wang, C.S. Qiu, J.E. Huettner, and M. Zhuo Direct presynaptic regulation of GABA/glycine release by kainate receptors in the dorsal horn: an ionotropic mechanism Neuron 32 2001 477 488
25. G.A. Kerchner, T.J. Wilding, P. Li, M. Zhuo, and J.E. Huettner Presynaptic kainate receptors regulate spinal sensory transmission J Neurosci 21 2001 59 66
26. Y.H. Kim, C.K. Park, S.K. Back, C.J. Lee, S.J. Hwang, Y.C. Bae, H.S. Na, J.S. Kim, S.J. Jung, and S.B. Oh Membrane-delimited coupling of TRPV1 and mGluR5 on presynaptic terminals of nociceptive neurons J Neurosci 29 2009 10000 10009
27. N. Kumar, A. Laferriere, J.S. Yu, T. Poon, and T.J. Coderre Metabotropic glutamate receptors (mGluRs) regulate noxious stimulus-induced glutamate release in the spinal cord dorsal horn of rats with neuropathic and inflammatory pain J Neurochem 114 2010 281 290
28. R. Kuner Central mechanisms of pathological pain Nat Med 16 2010 1258 1266
29. A. Latremoliere, and C.J. Woolf Central sensitization: a generator of pain hypersensitivity by central neural plasticity J Pain 10 2009 895 926
30. C.J. Lee, R. Bardoni, C.K. Tong, H.S. Engelman, D.J. Joseph, P.C. Magherini, and A.B. MacDermott 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. J.Q. Li, S.R. Chen, H. Chen, Y.Q. Cai, and H.L. Pan Regulation of increased glutamatergic input to spinal dorsal horn neurons by mGluR5 in diabetic neuropathic pain J Neurochem 112 2010 162 172
32. C.N. Liu, P.D. Wall, E. Ben-Dor, M. Michaelis, R. Amir, and M. Devor Tactile allodynia in the absence of C-fiber activation: altered firing properties of DRG neurons following spinal nerve injury PAIN® 85 2000 503 521
33. H. Liu, P.W. Mantyh, and A.I. Basbaum NMDA-receptor regulation of substance P release from primary afferent nociceptors Nature 386 1997 721 724
34. X. Liu, S. Eschenfelder, K.H. Blenk, W. Janig, and H. Habler Spontaneous activity of axotomized afferent neurons after L5 spinal nerve injury in rats PAIN® 84 2000 309 318
35. S. Maeda, A. Kawamoto, Y. Yatani, H. Shirakawa, T. Nakagawa, and S. Kaneko Gene transfer of GLT-1, a glial glutamate transporter, into the spinal cord by recombinant adenovirus attenuates inflammatory and neuropathic pain in rats Mol Pain 4 2008 65
36. C.R. McNamara, J. Mandel-Brehm, D.M. Bautista, J. Siemens, K.L. Deranian, M. Zhao, N.J. Hayward, J.A. Chong, D. Julius, M.M. Moran, and C.M. Fanger TRPA1 mediates formalin-induced pain Proc Natl Acad Sci USA 104 2007 13525 13530
37. M. Michaelis, X. Liu, and W. Janig Axotomized and intact muscle afferents but no skin afferents develop ongoing discharges of dorsal root ganglion origin after peripheral nerve lesion J Neurosci 20 2000 2742 2748
38. B.R. Miller, J.L. Dorner, M. Shou, Y. Sari, S.J. Barton, D.R. Sengelaub, R.T. Kennedy, and G.V. Rebec Up-regulation of GLT1 expression increases glutamate uptake and attenuates the Huntington's disease phenotype in the R6/2 mouse Neuroscience 153 2008 329 337
39. K.E. Miller, E.M. Hoffman, M. Sutharshan, and R. Schechter Glutamate pharmacology and metabolism in peripheral primary afferents: physiological and pathophysiological mechanisms Pharmacol Ther 130 2011 283 309
40. V. Neugebauer Metabotropic glutamate receptors - important modulators of nociception and pain behavior PAIN® 98 2002 1 8
41. H. Nie, and H.R. Weng Impaired glial glutamate uptake induces extrasynaptic glutamate spillover in the spinal sensory synapses of neuropathic rats J Neurophysiol 103 2010 2570 2580
42. H. Nie, H. Zhang, and H.R. Weng Minocycline prevents impaired glial glutamate uptake in the spinal sensory synapses of neuropathic rats Neuroscience 170 2010 901 912
43. E. Niederberger, A. Schmidtko, J.D. Rothstein, G. Geisslinger, and I. Tegeder Modulation of spinal nociceptive processing through the glutamate transporter GLT-1 Neuroscience 116 2003 81 87
44. C.M. Niswender, and P.J. Conn Metabotropic glutamate receptors: physiology, pharmacology, and disease Annu Rev Pharmacol Toxicol 50 2010 295 322
45. P.S. Pinheiro, and C. Mulle Presynaptic glutamate receptors: physiological functions and mechanisms of action Nat Rev Neurosci 9 2008 423 436
46. M.H. Pitcher, A. Ribeiro-da-Silva, and T.J. Coderre Effects of inflammation on the ultrastructural localization of spinal cord dorsal horn group I metabotropic glutamate receptors J Comp Neurol 505 2007 412 423
47. K. Pozo, and Y. Goda Unraveling mechanisms of homeostatic synaptic plasticity Neuron 66 2010 337 351
48. K.M. Ramos, M.T. Lewis, K.N. Morgan, N.Y. Crysdale, J.L. Kroll, F.R. Taylor, J.A. Harrison, E.M. Sloane, S.F. Maier, and L.R. Watkins Spinal upregulation of glutamate transporter GLT-1 by ceftriaxone: therapeutic efficacy in a range of experimental nervous system disorders Neuroscience 169 2010 1888 1900
49. J.D. Rothstein, L. Martin, A.I. Levey, M. Dykes-Hoberg, L. Jin, D. Wu, N. Nash, and R.W. Kuncl Localization of neuronal and glial glutamate transporters Neuron 13 1994 713 725
50. J.D. Rothstein, L.J. Martin, and R.W. Kuncl Decreased glutamate transport by the brain and spinal cord in amyotrophic lateral sclerosis N Engl J Med 326 1992 1464 1468
51. J.D. Rothstein, S. Patel, M.R. Regan, C. Haenggeli, Y.H. Huang, D.E. Bergles, L. Jin, M. Dykes Hoberg, S. Vidensky, D.S. Chung, S.V. Toan, L.I. Bruijn, Z.Z. Su, P. Gupta, and P.B. Fisher Beta-lactam antibiotics offer neuroprotection by increasing glutamate transporter expression Nature 433 2005 73 77
52. J. Sandkühler Models and mechanisms of hyperalgesia and allodynia Physiol Rev 89 2009 707 758
53. J. Scholz, A. Abele, C. Marian, A. Haussler, T.A. Herbert, C.J. Woolf, and I. Tegeder Low-dose methotrexate reduces peripheral nerve injury-evoked spinal microglial activation and neuropathic pain behavior in rats PAIN® 138 2008 130 142
54. K. Shimamoto, B. Lebrun, Y. Yasuda-Kamatani, M. Sakaitani, Y. Shigeri, N. Yumoto, and T. Nakajima DL-threo-beta-benzyloxyaspartate, a potent blocker of excitatory amino acid transporters Mol Pharmacol 53 1998 195 201
55. B. Sung, G. Lim, and J. Mao Altered expression and uptake activity of spinal glutamate transporters after nerve injury contribute to the pathogenesis of neuropathic pain in rats J Neurosci 23 2003 2899 2910
56. Y. Takasugi, T. Shirai, K. Futagawa, Y. Koga, K. Egawa, S. Watanabe, and T. Umeda Transcutaneous cisternal puncture for sampling of cerebrospinal fluid in awake rat Exp Anim 54 2005 193 196
57. Y.X. Tao, J. Gu, and R.L. Stephens Jr. Role of spinal cord glutamate transporter during normal sensory transmission and pathological pain states Mol Pain 1 2005 30
58. A.J. Todd Neuronal circuitry for pain processing in the dorsal horn Nat Rev Neurosci 11 2010 823 836
59. A.V. Tzingounis, and J.I. Wadiche Glutamate transporters: confining runaway excitation by shaping synaptic transmission Nat Rev Neurosci 8 2007 935 947
60. G. Vetter, G. Geisslinger, and I. Tegeder Release of glutamate, nitric oxide and prostaglandin E2 and metabolic activity in the spinal cord of rats following peripheral nociceptive stimulation PAIN® 92 2001 213 218
61. K. Walker, A. Reeve, M. Bowes, J. Winter, G. Wotherspoon, A. Davis, P. Schmid, F. Gasparini, R. Kuhn, and L. Urban MGlu5 receptors and nociceptive function II. mGlu5 receptors functionally expressed on peripheral sensory neurones mediate inflammatory hyperalgesia Neuropharmacology 40 2001 10 19
62. W. Xie, J.A. Strong, J.T. Meij, J.M. Zhang, and L. Yu Neuropathic pain: early spontaneous afferent activity is the trigger PAIN® 116 2005 243 256
63. W.J. Xin, H.R. Weng, and P.M. Dougherty Plasticity in expression of the glutamate transporters GLT-1 and GLAST in spinal dorsal horn glial cells following partial sciatic nerve ligation Mol Pain 5 2009 15
64. M. Yaster, X. Guan, R.S. Petralia, J.D. Rothstein, W. Lu, and Y.X. Tao Effect of inhibition of spinal cord glutamate transporters on inflammatory pain induced by formalin and complete Freund's adjuvant Anesthesiology 114 2011 412 423
65. Y. Zhang, and B.A. Barres Astrocyte heterogeneity: an underappreciated topic in neurobiology Curr Opin Neurobiol 20 2010 588 594
66. C.Z. Zhu, S.G. Wilson, J.P. Mikusa, C.T. Wismer, D.M. Gauvin, J.J. Lynch 3rd, C.L. Wade, M.W. Decker, and P. Honore Assessing the role of metabotropic glutamate receptor 5 in multiple nociceptive modalities Eur J Pharmacol 506 2004 107 118