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

Journal of Neurotrauma

Volumn 27, Issue 12, 2010, Pages 2261-2271

  Weisshaar, Christine L ^a   Dong, Ling ^b   Bowman, Alex S ^c   Perez, Federico M ^c   Guarino, Benjamin B ^b   Sweitzer, Sarah M ^c   Winkelstein, Beth A ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

adolescent; glia; glutamate; pain; protein kinase C

Indexed keywords

METABOTROPIC RECEPTOR 5; PROTEIN KINASE C EPSILON;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR; BIOMECHANICS; CELL ACTIVATION; CONTROLLED STUDY; GLIA CELL; HYPERALGESIA; HYPERSENSITIVITY; IMMUNOHISTOCHEMISTRY; MALE; NECK INJURY; NERVE CELL; NONHUMAN; PROTEIN EXPRESSION; RAT; SPINAL GANGLION;

ANALYSIS OF VARIANCE; ANIMALS; CELL COUNT; GANGLIA, SPINAL; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; MALE; NECK INJURIES; NECK PAIN; NEUROGLIA; NEURONS; PHYSICAL STIMULATION; PROTEIN KINASE C-EPSILON; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, METABOTROPIC GLUTAMATE; ZYGAPOPHYSEAL JOINT;

EID: 78650080975     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2010.1460     Document Type: Article

References (83)

1. Ahlgren, S., and Levine, J. (1994). Protein kinase C inhibitors decrease hyperalgesia and c-fiber excitability in the strepto-zotocin-diabetic rat. J. Neurophys. 72, 684-692.
2. Amadesi, S., Cottrell, G., Divino, L., Chapman, K., Grady, E., Bautista, F., Karanjia, R., Barajas-Lopez, C., Vanner, S., Verg-nolle, N., and Bunnett, N. (2006). Protease-activated receptor 2 sensitizes TRPV1 by protein kinase C-epsilon-and A-depen-dent mechanisms in rats and mice. J. Physiol. 575, 555-571.
3. Aprill, C., and Bogduk, N. (1992). The prevalence of cervical zygapophyseal joint pain. A first approximation. Spine 17, 744-747.
4. Balagué, F., Dutoit, G., and Waldburger, M. (1998). Low back pain in schoolchildren. An epidemiological study. Scand. J. Rehabil. Med. 20, 175-179.
5. Balagué, F., Skovron, M., Nordin, M., Dutoit, G., Pol, L., and Waldburger, M. (1995). Low back pain in schoolchildren. A study of familial and psychological factors. Spine 20, 1265-1270.
6. Barnsley, L., Lord, S., and Bogduk, N. (1994). Whiplash injury. Pain 58, 283-307.
7. Barnsley, L., Lord, S., Wallis, B., and Bogduk, N. (1995). The prevalence of chronic cervical zygapophysial joint pain after whiplash. Spine 20, 20-25.
8. Bergman E., and Ulfhake B. (1998). Loss of primary sensory neurons in the very old rat: neuron number estimates using the dissector method and confocal optical sectioning. J. Comp. Neurol. 396, 211-222.
9. Bhave, G., Karim, F., Carlton, S., and Gereau, R. (2001). Peripheral group I metabotropic glutamate receptors modulate nociception in mice. Nat. Neurosci. 4, 417-423.
10. Bogduk, N., and Marsland, A. (1988). The cervical zygapophy-sial joints as a source of neck pain. Spine 13, 610-617.
11. Carlton, S.M., and Hargett, G.L. (2007). Colocalization of meta-botropic glutamate receptors in rat dorsal root ganglion cells. J. Comp. Neurol. 501, 780-789.
12. Chaplan, S., Bach, F., Pogrel, J., Chung, J., and Yaksh, T. (1994). Quantitative assessment of tactile allodynia in the rat paw. J. Neurosci. Methods 53, 55-63.
13. Cheung, C., Shum, S., Tang, S. Yau, P., and Chiu, T. (2009). The correlation between craniovertebral angle, backpack weights, and disability due to neck pain in adolescents. J. Back Mus-culoskelet. Rehabil. 22, 197-203.
14. Colburn, R., Rickman, A., and DeLeo, J. (1999). The effect of site and type of nerve injury on spinal glial activation and neuropathic pain behavior. Exp. Neurol. 157, 289-304.
15. Conn, P., and Pin, J. (1997). Pharmacology and functions of metabotropic glutamate receptors. Ann. Rev. Pharmacol. Toxicol. 37, 205-237.
16. Decosterd, I., and Woolf, C. (2000). Spared nerve injury: an animal model of persistent peripheral neuropathic pain. Pain 87, 149-158.
17. DeLeo, J., and Yezierski, R. (2001). The role of neuroinflamma-tion and neuroimmune activation in persistent pain. Pain 90, 1-6.
18. Deng, B., Begeman, P., Yang, K., Tashman, S., and King, A. (2000). Kinematics of human cadaver cervical spine during low speed rear-end impacts. Stapp Car Crash J. 44, 171-188.
19. Dina, O., Barletta, J., Chen, X., Mutero, A., Martin, A., Messing, R., and Levine, J. (2000). Key role for the epsilon isoform of protein kinase C in painful alcoholic neuropathy in the rat. J. Neurosci. 20, 8614-8619.
20. Dogrul, A., Ossipov, M.H., Lai, J., Malan, T., and Porreca, F. (2000). Peripheral and spinal antihyperalgesic activity of SIB-1757, a metabotropic glutamate receptor (mGluR(5)) antagonist, in experimental neuropathic pain in rats. Neurosci. Lett. 292, 115-118.
21. Dong, L., Odeleye, A., Jordan-Sciutto, K., and Winkelstein, B. (2008). Painful facet joint injury induces neuronal stress activation in the DRG: Implications for cellular mechanisms of pain. Neurosci. Lett. 443, 90-94.
22. Dong, L., and Winkelstein, B. (2010). Simulated whiplash modulates express of the glutamatergic system in the spinal cord suggesting spinal plasticity is associated with painful dynamic cervical facet loading. J. Neurotrauma 27, 163-174.
23. El-Metwally, A. (2004). Prognosis of non-specific musculoskele-tal pain in preadolescents: A prospective 4-year follow-up study till adolescence. Pain 110, 550-559.
24. Ferreira, J., Trichês, K., Medeiros, R., and Calixto, J. (2005). Mechanisms involved in the nociception produced by peripheral protein kinase c activation in mice. Pain 117, 171-181.
25. Grimmer, K., Nyland, L., and Milanese, S. (2006). Repeated measures of recent headache, neck and upper back pain in Australian adolescents. Cephalalgia 26, 843-851.
26. Grimmer, K., Williams, M., and Gill, T. (1999). The associations between adolescent head-on-neck posture, backpack weight, and anthropometric features. Spine 24, 2262-2267.
27. Gwak, Y., and Hulsebosch, C. (2005). Upregulation of group I metabotropic glutamate receptors in neurons and astrocytes in the dorsal horn following spinal cord injury. Exp. Neurol. 195, 236-243.
28. Hall, T., and Robinson, K. (2004). The flexion-rotation test and active cervical mobility\a comparative measurement study in cervicogenic headache. Man. Ther. 9, 197-202.
29. Hama, A. (2003). Acute activation of the spinal cord metabo-tropic glutamate subtype-5 receptor leads to cold hypersen-sitivity in the rat. Neuropharmacology 44, 423-430.
30. Hertzberg, A. (1985). Prediction of cervical and low-back pain based on routine school health examinations. A nine-to twelve-year follow-up study. Scand. J. Prim. Health Care 3, 247-253.
31. Hubbard, R., and Winkelstein, B. (2005). Transient cervical nerve root compression in the rat induces bilateral forepaw allody-nia and spinal glial activation: Mechanical factors in painful neck injuries. Spine 30, 1924-1932.
32. Hudson, L., Bevan, S., McNair, K., Gentry, C., Fox, A., Kuhn, R., and Winter, J. (2002). Metabotropic glutamate receptor 5 up-regulation in A-fibers after spinal nerve injury: 2-methyl-6-(phenylethynyl)-pyridine (MPEP) reverses the induced thermal hyperalgesia. J. Neurosci. 22, 2660-2668.
33. Jull, G., Amiri, M., Bullock-Saxton, J., Darnell, R., and Lander, C. (2007). Cervical musculoskeletal impairment in frequent intermittent headache. Part 1: Subjects with single headaches. Cephalalgia 27, 793-802.
34. Kaneoka, K., Ono, K., Inami, S., and Hayashi, K. (1999). Motion analysis of cervical vertebrae during whiplash loading. Spine 24, 763-769.
35. Karim, F., Wang, C., and Gereau, R. (2001). Metabotropic glu-tamate receptor subtypes 1 and 5 are activators of extracellular signal-related kinase signaling required for inflammatory pain in mice. J. Neurosci. 21, 3771-3779.
36. Khasar, S., Lin, Y., Martin, A., Dadgar, J., McMahon, T., Wang, D., Hundle, B., Aley, K., Isenberg, W., McCarter, G., Green, P., Hodge, C., Levine, J., and Messing, R. (1999). A novel noci-ceptor signaling pathway revealed in protein kinase C epsilon mutant mice. Neuron 24, 253-260.
37. Kim, Y., Park, C., Back, S., Lee, C., Hwang, S., Bae, Y., Na, H., Kim, J., Jung, S., and Oh, S. (2009). Membrane-delimited coupling of TRPV1 and mGluR5 on presynaptic terminals of nociceptive neurons. J. Neurosci. 29, 10000-10009.
38. Korovessis, P., Koureas, G., and Papazisis, Z. (2004). Correlation between backpack weight and way of carrying, sagittal and frontal spinal curvatures, athletic activity, and dorsal and low back pain in schoolchildren and adolescents. J. Spinal Disord. Tech. 17, 33-40.
39. Kristánsdó ttir, G. (1996) Prevalence of self-reported back pain in school children: A study of sociodemographic differences. Eur. J. Pediatr. 155. 984-986.
40. Leboeuf-Yde, C., and Kyvik, K. (1998). At what age does low back pain become a common problem?: A study of 29,424 individuals aged 12-41 years. Spine 23, 228-234.
41. Lee, J., and Ro, J. (2007). Peripheral metabotropic glutamate receptor 5 mediates mechanical hypersensitivity in craniofacial muscle via protein kinase C dependent mechanisms. Neu-roscience 146, 375-383.
42. Lee, K., Davis, M., Mejilla, R., and Winkelstein, B. (2004a). In vivo cervical facet capsule distraction: mechanical implications for whiplash and neck pain. Stapp Car Crash J. 48, 373-395.
43. Lee, K., Davis, M., and Winkelstein, B. (2008). Capsular ligament involvement in the development of mechanical hyperalgesia after facet joint loading: behavioral and inflammatory outcomes in a rodent model of pain. J. Neurotrauama 25, 1383-1393.
44. Lee, K., Franklin, A., Davis, M., and Winkelstein, B. (2006). Tensile cervical facet capsule ligament mechanics: Failure and subfailure responses in the rat. J. Biomech. 39, 1256-1264.
45. Lee, K., Thinnes, J., Gokhin, D., and Winkelstein, B. (2004b). A novel rodent neck pain model of facet-mediated behavioral hypersensitivity: implications for persistent pain and whiplash injury. J. Neurosci. Methods 137, 151-159.
46. Lee, K., and Winkelstein, B. (2009). Joint distraction magnitude is associated with different behavioral outcomes and substance P levels for cervical facet joint loading in the rat. J. Pain 10, 436-445.
47. Liang, Y., Huang, C., and Hsu, K. (2005). Characterization of long-term potentiation of primary afferent transmission at trigeminal synapses of juvenile rats: essential role of subtype 5 metabotropic glutamate receptors. Pain 114, 417-428.
48. Luan, F., Yang, K., Deng, B., Begeman, P., Tashman, S., and King, A. (2000). Qualitative analysis of neck kinematics during low-speed rear-end impact. Clin. Biomech. 15, 649-657.
49. Lu, Y., Chen, C., Kallakuri, S., Patwardhan, A., and Cavanaugh, J. (2005b). Neural response of cervical facet joint capsule to stretch: A study of whiplash pain mechanism. Stapp Car Crash J. 49, 49-65.
50. Lu, Y., Chen, C., Kallakuri, S., Patwardhan, A., and Cavanaugh, J. (2005a). Neurophysiological and biomechanical characterization of goat cervical facet joint capsules. J. Orthop. Res. 23, 779-787.
51. Mills, C., Xu, G., Johnson, K., McAdoo, D., and Hulsebosch, C. (2000). AIDA reduces glutamate release and attenuates mechanical allodynia after spinal cord injury. Neuroreport 11, 3067-3070.
52. Morenilla-Palao, C., Planells-Cases, R., Garć?a-Sanz, N., and Ferrer-Montiel, A. (2004). Regulated exocytosis contributes to protein kinase C potentiation of vanilloid receptor activity. J. Biol. Chem. 279, 25665-25672.
53. Newman, E. (2003). New roles for astrocytes: regulation of synaptic transmission. Trends Neurosci. 26, 536-542.
54. Ono, K., Kaneoka, K., Wittek, A., and Kajzer, J. (1997). Cervical injury mechanism based on the analysis of human cervical vertebral motion and head-neck-torso kinematics during low speed rear impacts. Stapp Car Crash J. 41, 339-356.
55. Osikowicz, M., Skup, M., Mika, J., Makuch, W., Czarkowska-Bauch, J., and Przewlocka, B. (2009). Glial inhibitors influence the mRNA and protein levels of mGlu2/3, 5 and 7 receptors and potentiate the analgesic effects of their ligands in a mouse model of neuropathic pain. Pain 147, 175-186.
56. Panjabi, M., Cholewicki, J., Nibu, K., Grauer, J., and Vahldiek, M. (1998). Capsular ligament stretches during in vitro whiplash simulations. J. Spinal Disord. 11, 227-232.
57. Pearson, A., Ivancic, P., Ito, S., and Panjabi, M. (2004). Facet joint kinematics and injury mechanisms during simulated whiplash. Spine 29, 390-397.
58. Pitcher, M., Ribeiro-da-Silva, A., Coderre, T. (2007). Effects of inflammation on the ultrastructural localization of spinal cord dorsal horn group I metabotrophic glutamate receptors. J. Comp. Neurol. 505, 412-423.
59. Rothman, S., Hubbard, R., Lee, K., and Winkelstein, B. (2008). Detection, transmission, and perception of pain, in: Interven-tional Spine: An Algorithmic Approach. C. Slipman, F. Simeone, and R. Derby (eds). Elsevier: Philadelphia, pps. 29-37.
60. Rutkowski, M., and DeLeo, J. (2002). The role of cytokines in the initiation and maintenance of chronic pain. Drug News Per-spect. 15, 626-632.
61. Schoepp, D., Jane, D., and Monn, J. (1999). Pharmacological agents acting at subtypes of metabotropic glutamate receptors. Neuropharmacology 38, 1431-1476.
62. Shumilla, J., Liron, T., Mochly-Rosen, D., Kendig, J., and Sweitzer, S. (2005). Ethanol withdrawal-associated allodynia and hyperalgesia: age-dependent regulation by protein kinase C epsilon and gamma isoenzymes. J. Pain 6, 535-549.
63. Sheir-Neiss, G., Kruse, R., Rahman, T., Jacobson, L., and Pelli, J. (2003). The association of backpack use and back pain in adolescents. Spine 28, 922-930.
64. Sjaastad, O., Fredriksen, T., Petersen, H., and Bakketeig, L. (2003). Features indicative of cervical abnormality. A factor to be reckoned with in clinical headache work and research? Funct. Neurol. 18, 195-203.
65. Souza, A., Moreira, F., Almeida, K., Bertollo, C., Costa, K., and Coelho, M. (2002). In vivo evidence for a role of protein kinase C in peripheral nociceptive processing. Br. J. Pharmacol. 135, 239-247
66. Sta?hl, M., Kautiainen, H., El-Metwally, A., Häkkinen, A., Ylinen, J., Salminen, J., and Mikkelsson, M. (2008). Non-specific neck pain in schoolchildren: prognosis and risk factors for occurrence and persistence. A 4-year follow-up study. Pain 137, 316-322.
67. Stemper, B., Yoganandan, N., and Pintar, F. (2005). Effects of abnormal posture on capsular ligament elongations in a computational model subjected to whiplash loading. J. Bio-mech. 38, 1313-1323.
68. Sundararajan, S., Prasad, P., Demetropoulos, C., Tashman, S., Begeman, P., Yang, K., and King, A. (2004). 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, 331-372.
69. Sweitzer, S., Shumilla, J., Zissen, M., and Kendig, J. (2003). Protein kinase c e and g: roles in age-specific modulation of acute opioid-withdrawal allodynia. Seminars Pain Med. 1, 206-219.
70. Sweitzer, S., Wong, S., Peters, M., Mochly-Rosen, D., Yeomans, D., and Kendig, J. (2004a). Protein kinase C epsilon and gamma: involvement in formalin-induced nociception in neonatal rats. J. Pharmacol. Exp. Ther. 309, 616-625.
71. Sweitzer, S., Wong, S., Tjolsen, A., Allen, C., Mochly-Rosen, D., and Kendig, J. (2004b). Exaggerated nociceptive responses on morphine withdrawal: roles of protein kinase C epsilon and gamma. Pain 110, 281-289.
72. Taimela, S., Kujala, U., Salminen, J., and Viljanen, T. (1997). The prevalence of low back pain among children and adolescents: a nationwide, cohort-based questionnaire survey in Finland. Spine 22, 1132-1136.
73. Velázquez, K., Mohammad, H., and Sweitzer, S. (2007). Protein kinase C in pain: involvement of multiple isoforms. Pharmacol. Res. 55, 578-589.
74. Walker, K., Bowes, M., Panesar, M., Davis, A., Gentry, C., Ke-singland, A., Gasparini, F., Spooren, W., Stoehr, N., Pagano, A., Flor, P., Vranesic, I., Lingenhoehl, K., Johnson, E., Varney, M., Urban, L., and Kuhn, R. (2001a). 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, 1-9.
75. Walker, K., Reeve, A., Bowes, M., Winter, J., Wotherspoon, G., Davis, A., Schmid, P., Gasparini, F., Kuhn, R., and Urban, L. (2001b). mGlu5 receptors and nociceptive function II. mGlu5 receptors functionally expressed on peripheral sensory neurons mediate inflammatory hyperalgesia. Neuropharmacology 40, 10-19.
76. Watkins, L., Milligan, E., and Maier, S. (2001). Glial activation: a driving force for pathological pain. Trends Neurosci. 24, 450-455.
77. Weber Hellstenius, S. (2009). Recurrent neck pain and headaches in preadolescents associated with mechanical dysfunction of the cervical spine: a cross-sectional observational study with 131 students. J. Manipulative Physiological Therapeutics 32, 625-634.
78. Winkelstein, B., and Santos, D. (2008). An intact facet capsular ligament modulates behavioral sensitivity and spinal glial activation produced by cervical facet joint tension. Spine 33, 856-862.
79. Yoganandan, N., Cusick, J., Pintar, F., and Rao, R. (2001). Whiplash injury determination with conventional spine imaging and cryomicrotomy. Spine 26, 2443-2448.
80. Yoganandan, N., Pintar, F., and Cusick, J. (2002). Biomechanical analyses of whiplash injuries using an experimental model. Accid. Anal. Prev. 34, 663-671.
81. Yoganandan, N., Pintar, F., and Klienberger, M. (1998). Cervical spine vertebral and facet joint kinematics under whiplash. J. Biomech. Eng. 120, 305-307.
82. Zimmerman, M. (1983). Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16, 109-110.
83. Zonta, M., Sebelin, A., Gobbo, S., Fellin, T., Pozzan, T., and Carmignoto, G. (2003). Glutamate-mediated cytosolic calcium oscillations regulate a pulsatile prostaglandin release from cultured rat astrocytes. J. Physiol. 553, 407-414.