PAIN
Volume 145, Issue 1 , Pages 151-159 , September 2009

Experimental arthritis causes tumor necrosis factor-α-dependent infiltration of macrophages into rat dorsal root ganglia which correlates with pain-related behavior

  • Gisela Segond von Banchet

      Affiliations

    • Institute of Physiology I, University Hospital Jena, Germany
    • Corresponding Author InformationCorresponding author. Address: University Hospital Jena, Institute of Physiology I/Neurophysiology, Teichgraben 8, D-07743 Jena, Germany. Tel.: +49 3641 938809; fax: +49 3641 938812.
    • ,
  • Michael K. Boettger

      Affiliations

    • Institute of Physiology I, University Hospital Jena, Germany
    • ,
  • Nadja Fischer

      Affiliations

    • Institute of Physiology I, University Hospital Jena, Germany
    • ,
  • Mieczyslaw Gajda

      Affiliations

    • Institute of Pathology, University Hospital Jena, Germany
    • ,
  • Rolf Bräuer

      Affiliations

    • Institute of Pathology, University Hospital Jena, Germany
    • ,
  • Hans-Georg Schaible

      Affiliations

    • Institute of Physiology I, University Hospital Jena, Germany

Received 7 November 2008 ,Revised 6 May 2009 ,Accepted 1 June 2009.

References 

  1. Boettger MK, Hensellek S, Richter F, Gajda M, Stöckigt R, Segond von Banchet G, et al. Antinociceptive effects of TNF-α neutralization in a rat model of antigen-induced arthritis. Evidence for a neuronal target. Arthritis Rheum. 2008;58:2368–2378
  2. Boettger MK, Üceyler N, Zelenka M, Schmitt A, Reif A, Chen Y, et al. Differences in inflammatory pain in nNOS-, iNOS- and eNOS-deficient mice. Eur J Pain. 2007;11:810–818
  3. Buchner E, Bräuer R, Emmrich F, Kinne RW. Induction of flare-up reactions in rat antigen-induced arthritis. J Autoimmun. 1995;8:61–74
  4. Damoiseaux JGMC, Dopp EA, Calame W, Chao D, MacPerson GG, Dijkstra CD. Rat macrophage lysosomal membrane antigen recognized by monoclonal antibody ED. Immunology. 1994;83:140–147
  5. Darren JK, Chanty A, Gow RM, Zhang Y, Gibert RE. Protein kinase Cβ inhibition attenuates osteopontin expression, macrophage recruitment, and tubulointerstitial injury in advanced experimental diabetic nephropathy. J Am Soc Nephrol. 2005;16:1654–1660
  6. Dijkstra CD, Dopp EA, van den Berg TK, Damoiseaux JG. Monoclonal antibodies against rat macrophages. J Immunol Methods. 1994;174:21–23
  7. Dubový P, Tučková R, Jančálek R, Svíženská I, Klusáková I. Increased invasion of ED-1 positive macrophages in both ipsi- and contralateral dorsal root ganglia following unilateral nerve injuries. Neurosci Lett. 2007;427:88–93
  8. Griffiths RJ. Characterisation and pharmacological sensitivity of antigen arthritis induced by methylated bovine serum albumin in the rat. Agents Actions. 1992;35:88–95
  9. Henninger DD, Panes J, Eppihimer M, Russell J, Gerritsen M, Anderson DC, et al. Cytokine-induced VCAM-1 and ICAM-1 expression in different organs of the mouse. J Immunol. 1997;158:1825–1832
  10. Henseleit U, Steinbrink K, Sunderkotter C, Goebeler M, Roth J, Sorg C. Expression of murine VCAM-1 in vitro and in different models of inflammation in vivo: correlation with immigration of monocytes. Exp Dermatol. 1994;3:249–256
  11. Hensellek S, Brell P, Schaible H-G, Bräuer R, Segond von Banchet G. The cytokine TNFα increases the proportion of DRG neurones expressing the TRPV1 receptor via the TNFR1 receptor and ERK activation. Mol Cell Neurosci. 2007;36:381–391
  12. Hu P, Bembrick AL, Keay KA, McLachlan EM. Immune cell involvement in dorsal root ganglia and spinal cord after chronic constriction or transection of the rat sciatic nerve. Brain Behav Immun. 2007;21:599–616
  13. Hu P, McLachlan EM. Macrophage and lymphocyte invasion of dorsal root ganglia after peripheral nerve lesions in the rat. Neuroscience. 2002;112:23–38
  14. Huey PU, Waugh KC, Etienne J, Eckel RH. Lipoprotein lipase is expressed in rat sciatic nerve and regulated in response to crush injury. J Lipid Res. 2002;43:19–25
  15. Inglis J, Nissim A, Lees DM, Hunt SP, Chernajovsky Y, Kidd BL. The differential contribution of tumour necrosis factor to thermal and mechanical hyperalgesia during chronic inflammation. Arthritis Res Ther. 2005;7:R807–R816
  16. Inglis J, Notley CA, Essex D, Wilson AW, Feldmann M, Anand P, et al. Collagen-induced arthritis as a model of hyperalgesie: functional and cellular analysis of the analgesic actions of tumor necrosis factor blockade. Arthritis Rheum. 2007;56:4015–4023
  17. Inoue K, Zama T, Kamimoto T, Aoki R, Ikeda Y, Kimura H, et al. TNFα-induced ATF3 expression is bidirectionally regulated by the JNK and ERK pathways in vascular endothelial cells. Genes Cells. 2004;9:59–70
  18. Jin X, Gereau RW. Acute p38-mediated modulation of tetrodotoxin-resistant sodium channels in mouse sensory neurons by tumor necrosis factor-α. J Neurosci. 2006;26:246–255
  19. Junger H, Sorkin LS. Nociceptive and inflammatory effects of subcutaneous TNF alpha. Pain. 2000;85:145–151
  20. Kaplanski G, Marin V, Fabrigoule M, Boulay V, Benoliel AM, Bongrand P, et al. Thrombin-activated human endothelial cells support monocyte adhesion in vitro following expression of intercellular adhesion molecule-1 (ICAM-1; CD54) and vascular cell adhesion molecule-1 (VCAM-1; CD106). Blood. 1998;92:1259–1267
  21. Koltzenburg M, Wall PD, McMahon SB. Does the right side know what the left is doing?. Trends Neurosci. 1999;22:122–127
  22. Murata Y, Rydevik B, Takahashi K, Takahashi I, Olmarker K. Macrophage appearance in the epineurium and endoneurium of dorsal root ganglion exposed to nucleus pulposus. J Peripher Nerv Syst. 2004;9:158–164
  23. Nicol GD, Lopshire JC, Pafford CM. Tumor necrosis factor enhances the capsaicin sensitivity of rat sensory neurons. J Neurosci. 1997;17:975–982
  24. Obata K, Yamanaka H, Fukuoka T, Yi D, Tokunaga A, Hashimoto N, et al. Contribution of injured and uninjured dorsal root ganglion neurons to pain behavior and the changes in gene expression following chronic constriction injury of the sciatic nerve in rats. Pain. 2003;101:65–77
  25. Opree A, Kress M. Involvement of the proinflammatory cytokines tumor necrosis factor-alpha, IL-1 beta, and IL-6 but not IL-8 in the development of heat hyperalgesia: effects on heat-evoked calcitonin gene-related peptide release from rat skin. J Neurosci. 2000;20:6289–6293
  26. Özaktay AC, Kallakuri S, Takebayashi T, Cavanaugh JM, Asik I, DeLeo JA, et al. Effects of interleukin-1beta, interleukin-6, and tumor necrosis factor on sensitivity of dorsal root ganglion and peripheral receptive fields in rats. Eur Spine J. 2006;15:1529–1537
  27. Pollock J, McFarlane SM, Connell MC, Zehavi U, Vandenabeele P, MacEwan DJ, et al. TNF-alpha receptors simultaneously activate Ca2+ mobilisation and stress kinases in cultured sensory neurones. Neuropharmacology. 2002;42:93–106
  28. Schaible H-G, Grubb BD. Afferent and spinal mechanisms of joint pain. Pain. 1993;55:5–54
  29. Schäfers M, Sorkin LS, Geis C, Shubayev V. Spinal nerve ligation induces transient upregulation of tumor necrosis factor receptors 1 and 2 in injured and adjacent uninjured dorsal root ganglia in the rat. Neurosci Lett. 2003;347:179–182
  30. Segond von Banchet G, Petrow PK, Bräuer R, Schaible H-G. Monoarticular antigen-induced arthritis leads to pronounced bilateral upregulation of the expression of neurokinin 1 and bradykinin 2 receptors in dorsal root ganglion neurones of rats. Arthritis Res. 2000;2:424–427
  31. Shenker N, Haigh R, Roberts E, Mapp P, Harris N, Blake D. A review of contralateral responses to a unilateral inflammatory lesion. Rheumatology. 2003;42:1279–1286
  32. Shubayev VI, Myers RR. Axonal transport of TNF-alpha in painful neuropathy: distribution of ligand tracer and TNF receptors. J Neuroimmunol. 2001;114:48–56
  33. Sorkin LS, Xiao WH, Wagner R, Myers RR. Tumour necrosis factor-alpha induces ectopic activity in nociceptive primary afferent fibres. Neuroscience. 1997;81:255–262
  34. Tsujino H, Kondo E, Fukuoka T, Dai Y, Tokunaga A, Miki K, et al. Activating transcription factor 3 (ATF3) induction by axotomy in sensory and motoneurons: a novel neuronal marker of nerve injury. Mol Cell Neurosci. 2000;15:170–182
  35. Tsuzuki K, Kondo E, Fukuoka T, Yi D, Tsajiino H, Sakagami M, et al. Differential regulation of P2X(3) mRNA expression by peripheral nerve injury in intact and injured neurons in the rat sensory ganglia. Pain. 2001;91:351–360
  36. Wu TC. The role of vascular cell adhesion molecule-1 in tumor immune evasion. Cancer Res. 2007;67:6003–6006
  37. Yamate J. Heterogeneity of macrophage populations and myofibroblasts appearing in rat renal interstitial fibrosis. J Toxicol Pathol. 2007;20:185–195
  38. Yonekawa K, Harlan JM. Targeting leukocyte integrins in human diseases. J Leukoc Biol. 2005;77:129–140

PII: S0304-3959(09)00327-3

doi: 10.1016/j.pain.2009.06.002

PAIN
Volume 145, Issue 1 , Pages 151-159 , September 2009

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