Whiplash-like facet joint loading initiates glutamatergic responses in the DRG and spinal cord associated with behavioral hypersensitivity

Brain Research

Volumn 1461, Issue , 2012, Pages 51-63

  Dong, Ling ^a   Quindlen, Julia C ^a   Lipschutz, Daniel E ^a   Winkelstein, Beth A ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Facet; Glutamate receptor; Glutamate transporter; Mechanical hyperalgesia; Protein kinase C; Spinal cord

Indexed keywords

EXCITATORY AMINO ACID TRANSPORTER 3; METABOTROPIC RECEPTOR 5; PROTEIN KINASE C EPSILON;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIORAL HYPERSENSITIVITY; CONTROLLED STUDY; HYPERALGESIA; IMMUNOREACTIVITY; INJURY SEVERITY; MALE; NECK PAIN; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SHAM PROCEDURE; SPINAL CORD; SPINAL GANGLION; WHIPLASH INJURY; WHIPLASH LIKE FACET JOINT INJURY;

ANIMALS; EXCITATORY AMINO ACID TRANSPORTER 3; GANGLIA, SPINAL; MALE; PAIN; PAIN MEASUREMENT; PROTEIN KINASE C-EPSILON; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, METABOTROPIC GLUTAMATE; SPINAL CORD; WHIPLASH INJURIES; ZYGAPOPHYSEAL JOINT;

RATTUS;

EID: 84861794216     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2012.04.026     Document Type: Article

References (91)

1. C. Abbadie, J.L. Brown, P.W. Mantyh, and A.I. Basbaum Spinal cord substance P receptor immunoreactivity increases in both inflammatory and nerve injury models of persistent pain Neuroscience 70 1996 201 209
2. S.C. Ahlgren, and J.D. Levine Protein kinase C inhibitors decrease hyperalgesia and C-fiber hyperexcitability in the streptozotocin-diabetic rat J. Neurophysiol. 72 1994 684 692
3. C. Akay, K.A. Lindl, N. Shyam, B. Nabet, Y. Goenage-Vazguez, J. Ruzbarsky, Y. Wang, D.L. Kolson, and K.L. Jordan-Sciutto Activation status of integrated stress response pathways in neurons and astrocytes of HAND cortex Neuropathol. Appl. Neurobiol. 38 2012 175 200
4. + currents Biochem. Biophys. Res. Commun. 134 1986 1245 1253
5. F.J. Alvarez, R.M. Villalba, P.A. Carr, P. Grandes, and P.M. Somohano Differential distribution of metabotropic glutamate receptors 1a, 1b, and 5 in the rat spinal cord J. Comp. Neurol. 422 2000 464 487
6. S. Amadesi, G.S. Cottrell, L. Divino, K. Chapman, E.F. Grady, F. Bautista, R. Karanjia, C. Barajas-Lopez, S. Vanner, N. Vergnolle, and N.W. Bunnett Protease-activated receptor 2 sensitizes TRPV1 by protein kinase Cepsilon- and A-dependent mechanisms in rats and mice J. Physiol. 575 2006 555 571
7. A.I. Avramov, J.M. Cavanaugh, C.A. Ozaktay, T.V. Getchell, and A.I. King The effects of controlled mechanical loading on group-II, III, and IV afferent units from the lumbar facet joint and surrounding tissue. An in vitro study J. Bone Joint Surg. Am. 74 1992 1464 1471
8. G. Bhave, F. Karim, S.M. Carlton, and R.W.I.V. Gereau Peripheral group I metabotropic glutamate receptors modulate nociception in mice Nat. Neurosci. 4 2001 417 423
9. K.R. Byrnes, B. Stoica, D.J. Loane, A. Riccio, M.I. Davis, and A.I. Faden Metabotropic glutamate receptor 5 activation inhibits microglial associated inflammation and neurotoxicity Glia 57 2009 550 560
10. C. Caruso, M.C. Bottino, M. Pampillo, D. Pisera, G. Jaita, B. Duvilanski, A. Seilicovich, and M. Lasaga Glutamate induces apoptosis in anterior pituitary cells through group II metabotropic glutamate receptor activation Endocrinology 145 2004 4677 4684
11. J.M. Cavanaugh, A. el-Bohy, W.N. Hardy, T.V. Getchell, M.L. Getchell, and A.I. King Sensory innervation of soft tissues of the lumbar spine in the rat J. Orthop. Res. 7 1989 378 388
12. S.R. Chaplan, F.W. Bach, J.W. Pogrel, J.M. Chung, and T.L. Yaksh Quantitative assessment of tactile allodynia in the rat paw J. Neurosci. Methods 53 1994 55 63
13. F.A. Chaudhry, K.P. Lehre, M. van Lookeren Campagne, O.P. Ottersen, N.C. Danbolt, and J. Storm-Mathisen Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry Neuron 15 1995 711 720
14. C. Chen, Y. Lu, S. Kallakuri, A. Patwardhan, and J.M. Cavanaugh Distribution of A-delta and C-fiber receptors in the cervical facet joint capsule and their response to stretch J. Bone Joint Surg. Am. 88 2006 1807 1816
15. K.Y. Choi, K. Chang, J.M. Pickel, J.D. Badger II, and K.W. Roche Expression of the metabotropic glutamate receptor 5 (mGluR5) induces melanoma in transgenic mice Proc. Natl. Acad. Sci. U. S. A. 108 2011 15219 15224
16. P.J. Conn, and J.P. Pin Pharmacology and functions of metabotropic glutamate receptors Annu. Rev. Pharmacol. Toxicol. 37 1997 205 237
17. P.R. Croft, M. Lewis, A.C. Papageorgiou, E. Thomas, M.I. Jayson, G.J. Macfarlane, and A.J. Silman Risk factors for neck pain: a longitudinal study in the general population Pain 93 2001 317 325
18. N.D. Crosby, and B.A. Winkelstein Spinal neuronal hyperexcitability is induced within 1 day of a painful facet joint injury BMES Annual Mtg. 2011 #Thurs-1-5-D, Hartford, CT
19. B. Deng, P. Begeman, K. Yang, S. Tashman, and A. King Kinematics of human cadaver cervical spine during low speed rear-end impacts Stapp Car Crash J. 44 2000 171 188
20. S.A. Deriemer, J.A. Strong, K.A. Albert, P. Greengard, and L.K. Kaczmarek Enhancement of calcium current in Aplysia neurons by phorbol ester and protein kinase C Nature 313 1985 313 316
21. A. Di Castro, L.J. Drew, J.N. Wood, and P. Cesare Modulation of sensory neuron mechanotransduction by PKC- and nerve growth factor-dependent pathways Proc. Natl. Acad. Sci. U. S. A. 103 2006 4699 4704
22. O.A. Dina, J. Barletta, X. Chen, A. Mutero, A. Martin, R.O. Messing, and J.D. Levine Key role for the epsilon isoform of protein kinase C in painful alcoholic neuropathy in the rat J. Neurosci. 20 2000 8614 8619
23. R. Dingledine, and C.J. McBain Glutamate and aspartate G.J. Siegel, B.W. Agranoff, R.W. Albers, S.K. Fisher, M.D. Uhler, Basic Neurochemistry: Molecular, Cellular and Medical Aspects 1999 Lippincott-Raven Philadelphia 315 334
24. A. Dogrul, M.H. Ossipov, J. Lai, T.P. Malan Jr., and F. Porreca Peripheral and spinal antihyperalgesic activity of SIB-1757, a metabotropic glutamate receptor (mGLUR(5)) antagonist, in experimental neuropathic pain in rats Neurosci. Lett. 292 2000 115 118
25. L. Dong, and B.A. Winkelstein Simulated whiplash modulates expression of the glutamatergic system in the spinal cord suggesting spinal plasticity is associated with painful dynamic cervical facet loading J. Neurotrauma 27 2010 163 174
26. L. Dong, A.O. Odeleye, K.L. Jordan-Sciutto, and B.A. Winkelsten Painful facet injury induces neuronal stress activation in the DRG: implications for cellular mechanisms of pain Neurosci. Lett. 443 2008 90 94
27. L. Dong, B.B. Guarino, K.L. Jordan-Sciutto, and B.A. Winkelstein Activating transcription factor 4, a mediator of the integrated stress response, is increased in the dorsal root ganglia following painful facet joint distraction Neuroscience 193 2011 377 386
28. P.M. Dougherty, J. Palecek, V. Paleckova, L.S. Sorkin, and W.D. Willis The role of NMDA and non-NMDA excitatory amino acid receptors in the excitation of primate spinothalamic tract neurons by mechanical, chemical, thermal, and electrical stimuli J. Neurosci. 12 1992 3025 3041
29. J. Ferreira, K.M. Trichês, R. Medeiros, and J.B. Calixto Mechanisms involved in the nociception produced by peripheral protein kinase C activation in mice Pain 117 2005 171 181
30. K. Fisher, C. Lefebvre, and T.J. Coderre Antinociceptive effects following intrathecal pretreatment with selective metabotropic glutamate receptor compounds in a rat model of neuropathic pain Pharmacol. Biochem. Behav. 73 2002 411 418
31. S.D. Ginsberg, L.J. Martin, and J.D. Rothstein Regional deafferentation down-regulates subtypes of glutamate transporter proteins J. Neurochem. 65 1995 2800 2803
32. A.T. Hama Acute activation of the spinal cord metabotropic glutamate subtype-5 receptor leads to cold hypersensitivity in the rat Neuropharmacology 44 2003 423 430
33. Y. He, W.G. Janssen, J.D. Rothstein, and J.H. Morrison Differential synaptic localization of the glutamate transporter EAAC1 and glutamate receptor subunit GluR2 in the rat hippocampus J. Comp. Neurol. 418 2000 255 269
34. R.D. Hubbard, and B.A. Winkelstein Transient cervical nerve root compression in the rat induces bilateral forepaw allodynia and spinal glial activation: mechanical factors in painful neck injuries Spine 301 2005 1924 1932
35. R.D. Hubbard, and B.A. Winkelstein Dorsal root compression produces myelinated axonal degeneration near the biomechanical thresholds for mechanical behavioral hypersensitivity Exp. Neurol. 212 2008 482 489
36. 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
37. M.R. Hutchinson, Y. Shavit, P.M. Grace, K.C. Rice, S.F. Maier, and L.R. Watkins Exploring the neuroimmunopharmacology of opioids: an integrative review of mechanisms of central immune signaling and their implications for opioid analgesia Pharmacol. Rev. 63 2011 772 810
38. Y.J. Jong, V. Kumar, and K.L. O'Malley Intracellular metabotropic glutamate receptor 5 (mGluR5) activates signaling cascades distinct from cell surface counterparts J. Biol. Chem. 284 2009 35827 35838
39. Y. Kanai, C.P. Smith, and M.A. Hediger A new family of neurotransmitter transporters: the high-affinity glutamate transporters FASEB J. 7 1993 1450 1459
40. F. Karim, C.C. Wang, and R.W. Gereau Metabotropic glutamate receptor subtypes 1 and 5 are activators of extracellular signal-regulated kinase signaling required for inflammatory pain in mice J. Neurosci. 21 2001 3771 3779
41. P.S. Khalsa, A.H. Hoffman, and P. Grigg Mechanical states encoded by stretch-sensitive neurons in feline joint capsule J. Neurophysiol. 76 1996 175 187
42. S.G. Khasar, Y.H. Lin, A. Martin, J. Dadgar, T. McMahon, D. Wang, B. Hundle, K.O. Aley, W. Isenberg, G. McCarter, P.G. Green, C.W. Hodge, J.D. Levine, and R.O. Messing A novel nociceptor signaling pathway revealed in protein kinase C epsilon mutant mice Neuron 24 1999 253 260
43. 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
44. P.M. Lea IV, and A.I. Faden Modulation of metabotropic glutamate receptors as potential treatment for acute and chronic neurodegenerative disorders Drug News Perspect. 16 2003 513 522
45. J.S. Lee, and J.Y. Ro Peripheral metabotropic glutamate receptor 5 mediates mechanical hypersensitivity in craniofacial muscle via protein kinase C dependent mechanisms Neuroscience 146 2007 375 383
46. K.E. Lee, M.B. Davis, R.M. Mejilla, and B.A. Winkelstein In vivo cervical facet capsule distraction: mechanical implications for whiplash and neck pain Stapp Car Crash J. 48 2004 373 396
47. K.E. Lee, J.H. Thinnes, D.S. Gokhin, and B.A. Winkelstein A novel rodent neck pain model of facet-mediated behavioral hypersensitivity: implications for persistent pain and whiplash injury J. Neurosci. Methods 137 2004 151 159
48. K.E. Lee, A.N. Franklin, M.B. Davis, and B.A. Winkelstein Tensile cervical facet capsule ligament mechanics: failure and subfailure responses in the rodent J. Biomech. 39 2006 1256 1264
49. K.E. Lee, M.B. Davis, and B.A. Winkelstein Capsular ligament involvement in the development of mechanical hyperalgesia after facet joint loading: behavioral and inflammatory outcomes in a rodent model of pain J. Neurotrauma 25 2008 1383 1393
50. S. Leng, K. Mizumura, K. Koda, and T. Kumasawa Excitation and sensitization of the heat response induced by a phorbol ester in canine visceral polymodal receptors studied in vitro Neurosci. Lett. 206 1996 13 19
51. W. Li, and V. Neugebauer Differential roles of mGluR1 and mGluR5 in brief and prolonged nociceptive processing in central amygdala neurons J. Neurophysiol. 91 2004 13 24
52. D. Liu, W. Thangnipon, and D.J. McAdoo Excitatory amino acids rise to toxic levels upon impact injury to the rat spinal cord Brain Res. 547 1991 344 348
53. Y. Lu, C. Chen, S. Kallakuri, A. Patwardhan, and J.M. Cavanaugh Neurophysiological and biomechanical characterization of goat cervical facet joint capsules J. Orthop. Res. 23 2005 779 787
54. F. Luan, K.H. Yang, B. Deng, P.C. Begeman, S. Tashman, and A.I. King Qualitative analysis of neck kinematics during low-speed rear-end impact Clin. Biomech. 15 2000 649 657
55. D.J. McAdoo, G.Y. Xu, G. Robak, and M.G. Hughes Changes in amino acid concentrations over time and space around an impact injury and their diffusion through the rat spinal cord Exp. Neurol. 159 1999 538 544
56. S. Mense, and N.R. Prabhakar Spinal termination of nociceptive afferent fibres from deep tissues in the cat Neurosci. Lett. 66 1986 169 174
57. C.D. Mills, G.Y. Xu, D.J. McAdoo, and C.E. Hulsebosch Involvement of metabotropic glutamate receptors in excitatory amino acid and GABA release following spinal cord injury in rat J. Neurochem. 79 2001 835 848
58. + dependent glutamate transporters (EAAT1, EAAT2, and EAAT3) in primary astrocyte cultures: effect of oxidative stress Brain Res. 922 2001 21 29
59. M.M. Panjabi, J. Cholewicki, K. Nibu, L.B. Babat, and J. Dvorak Simulation of whiplash trauma using whole cervical spine specimens Spine 23 1998 17 24
60. A. Pearson, P.C. Ivancic, S. Ito, and M.M. Panjabi Facet joint kinematics and injury mechanisms during simulated whiplash Spine 29 2004 390 397
61. J.G. Pickar, and R.F. McLain Responses of mechanosensitive afferents to manipulation of the lumbar facet in the cat Spine 20 1995 2379 2385
62. J.P. Pin, and J. Bockaert Get receptive to metabotropic glutamate receptors Curr. Opin. Neurobiol. 5 1995 342 349
63. 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
64. K.P. Quinn, K.E. Lee, C.C. Ahaghotu, and B.A. Winkelstein Structural changes in the cervical facet capsular ligament: potential contributions to pain following subfailure loading Stapp Car Crash J. 51 2007 169 187
65. K.P. Quinn, L. Dong, F.J. Golder, and B.A. Winkelstein Neuronal hyperexcitability in the dorsal horn after painful facet joint injury Pain 151 2010 414 421
66. A.C. Rimaniol, P. Mialocq, P. Clayette, D. Dormont, and G. Gras Role of glutamate transporters in the regulation of glutathione levels in human macrophages Am. J. Physiol. Cell Physiol. 281 2001 C1964 C1970
67. S.M. Rothman, and B.A. Winkelstein Chemical and mechanical nerve root insults induce differential behavioral sensitivity and glial activation that are enhanced in combination Brain Res. 1181 2007 30 43
68. S.M. Rothman, and B.A. Winkelstein Cytokine antagonism reduces pain and modulates spinal astrocytic reactivity after cervical nerve root model of radiculopathy J. Neurotrauma 27 2010 803 814
69. J.D. Rothstein, M. Dykes-Hoberg, C.A. Pardo, L.A. Bristol, L. Jin, R.W. Kuncl, Y. Kanai, M.A. Hediger, Y. Wang, J.P. Schielke, and D.F. Welty Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate Neuron 16 1996 675 686
70. H.G. Schaible, A. Ebersberger, and G.S. Von Banchet Mechanisms of pain in arthritis Ann. N. Y. Acad. Sci. 966 2002 343 354 2002
71. K. Schepelmann, K. Meblinger, and R.F. Schmidt The effects of phorbol ester on slowly conducting afferents of the cat's knee joint Exp. Brain Res. 92 1993 391 398
72. D.D. Schoepp, D.E. Jane, and J.A. Monn Pharmacological agents acting at subtypes of metabotropic glutamate receptors Neuropharmacology 38 1999 1431 1476
73. P. Shashidharan, G.W. Huntley, J.M. Murray, A. Buku, T. Moran, M.J. Walsh, J.H. Morrison, and A. Plaitakis Immunohistochemical localization of the neuron-specific glutamate transporter EAAC1 (EAAT3) in rat brain and spinal cord revealed by a novel monoclonal antibody Brain Res. 773 1997 139 148
74. K.A. Sluka, and K.N. Westlund Behavioral and immunohistochemical changes in an experimental arthritis model in rats Pain 55 1993 367 377
75. A.L. Souza, F.A. Moreira, K.R. Almeida, C.M. Bertollo, K.A. Costa, and M.M. Coelho In vivo evidence for a role of protein kinase C in peripheral nociceptive processing Br. J. Pharmacol. 135 2002 239 247
76. B.D. Stemper, N. Yoganandan, T.A. Gennarelli, and F.A. Pintar Localized cervical facet joint kinematics under physiological and whiplash loading J. Neurosurg. Spine 3 2005 471 476
77. S. Sundararajan, P. Prasad, C.K. Demetropoulos, S. Tashman, P.C. Begeman, K.H. Yang, and A.I. King Effect of head-neck position on cervical facet stretch of post mortem human subjects during low speed rear end impacts Stapp Car Crash J. 48 2004 331 372
78. 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
79. S.M. Sweitzer, S.M. Wong, M.C. Peters, D. Mochly-Rosen, D.C. Yeomans, and J.J. Kendig Protein kinase C epsilon and gamma: involvement in formalin-induced nociception in neonatal rats J. Pharmacol. Exp. Ther. 309 2004 616 625
80. A.J. Todd Anatomy of primary afferents and projection neurons in the rat spinal dorsal horn with particular emphasis on substance P and the neurokinin 1 receptor Exp. Physiol. 87 2002 245 249
81. J.G. Valtschanoff, K.D. Phend, P.S. Bernardi, R.J. Weinberg, and A. Rustioni Amino acid immunocytochemistry of primary afferent terminals in the rat dorsal horn J. Comp. Neurol. 346 1994 237 252
82. L.P. Vera-Portocarrero, C.D. Mills, Z. Ye, S.D. Fullwood, D.J. McAdoo, C.E. Hulsebosch, and K.N. Westlund Rapid changes in expression of glutamate transporters after spinal cord injury Brain Res. 927 2002 104 110
83. K. Walker, M. Bowes, M. Panesar, A. Davis, C. Gentry, A. Kesingland, F. Gasparini, W. Spooren, N. Stoehr, A. Pagano, P.J. Flor, I. Vranesic, K. Lingenhoehl, E.C. Johnson, M. Varney, L. Urban, and R. Kuhn Metabotropic glutamate receptor subtype 5 (mGlu5) and nociceptive function. I. Selective blockade of mGlu5 receptors in models of acute, persistent and chronic pain Neuropharmacology 40 2001 1 9
84. Y.J. Wang, and G.F. Tseng Spinal axonal injury transiently elevates the level of metabotropic glutamate receptor 5, but not 1, in cord-projection central neurons J. Neurotrauma 21 2004 479 489
85. S. Wang, G. Lim, L. Yang, B. Sung, and J. Mao Downregulation of spinal glutamate transporter EAAC1 following nerve injury is regulated by central glucocorticoid receptors in rats Pain 120 2006 78 85
86. C.L. Weisshaar, L. Dong, A.S. Bowman, F.M. Perez, B.B. Guarino, S.M. Sweitzer, and B.A. Winkelstein Metabotropic glutamate receptor-5 and protein kinase C-epsilon increase in dorsal root ganglion neurons and spinal glial activation in an adolescent rat model of painful neck injury J. Neurotrauma 27 2010 2261 2271
87. T. Xu, W. Jiang, D. Du, Y. Xu, Q. Hu, and Q. Shen Role of spinal metabotropic glutamate receptor subtype 5 in the development of tolerance to morphine-induced antinociception in rat Neurosci. Lett. 420 2007 155 159
88. N. Yoganandan, F.A. Pintar, and M. Klienberger Cervical spine vertebral and facet joint kinematics under whiplash J. Biomech. Eng. 120 1998 305 307
89. N. Yoganandan, F.A. Pintar, and J.F. Cusick Biomechanical analyses of whiplash injuries using an experimental model Accid. Anal. Prev. 34 2002 663 671
90. H. Zhang, W. Xin, and P.M. Dougherty Synaptically evoked glutamate transporter currents in spinal dorsal horn astrocytes Mol. Pain 5 2009 36
91. M. Zimmermann Ethical guidelines for investigations of experimental pain in conscious animals Pain 16 1983 109 110