PAIN
Volume 151, Issue 2 , Pages 394-403 , November 2010

Characterization of the acute and persistent pain state present in K/BxN serum transfer arthritis

  • Christina A. Christianson

      Affiliations

    • Department of Pharmacology, University of California, San Diego, La Jolla, CA, USA
    • Department of Anesthesiology, University of California, San Diego, La Jolla, CA, USA
  • ,
  • Maripat Corr

      Affiliations

    • Division of Rheumatology, Allergy and Immunology, University of California, San Diego, La Jolla, CA, USA
  • ,
  • Gary S. Firestein

      Affiliations

    • Division of Rheumatology, Allergy and Immunology, University of California, San Diego, La Jolla, CA, USA
  • ,
  • Anahita Mobargha

      Affiliations

    • Department of Physiology and Pharmacology, Karolinska Institute, Stockholm, Sweden
  • ,
  • Tony L. Yaksh

      Affiliations

    • Department of Pharmacology, University of California, San Diego, La Jolla, CA, USA
    • Department of Anesthesiology, University of California, San Diego, La Jolla, CA, USA
  • ,
  • Camilla I. Svensson

      Affiliations

    • Department of Physiology and Pharmacology, Karolinska Institute, Stockholm, Sweden
    • Corresponding Author InformationCorresponding author. Tel.: +46 8 524 87948.

Received 7 May 2010 ,Revised 9 July 2010 ,Accepted 29 July 2010.

References 

  1. Boettger MK, Hensellek S, Richter F, Gajda M, Stockigt R, von Banchet GS, et al. Antinociceptive effects of tumor necrosis factor alpha neutralization in a rat model of antigen-induced arthritis: evidence of a neuronal target. Arthritis Rheum. 2008;58:2368–2378
  2. Butler SH, Godefroy F, Besson JM, Weil-Fugazza J. A limited arthritic model for chronic pain studies in the rat. Pain. 1992;48:73–81
  3. Calza L, Pozza M, Arletti R, Manzini E, Hokfelt T. Long-lasting regulation of galanin, opioid, and other peptides in dorsal root ganglia and spinal cord during experimental polyarthritis. Exp Neurol. 2000;164:333–343
  4. Cao H, Zhang YQ. Spinal glial activation contributes to pathological pain states. Neurosci Biobehav Rev. 2008;32:972–983
  5. Cervero F. Spinal cord hyperexcitability and its role in pain and hyperalgesia. Exp Brain Res. 2009;196:129–137
  6. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods. 1994;53:55–63
  7. Chen M, Boilard E, Nigrovic PA, Clark P, Xu D, Fitzgerald GA, et al. Predominance of cyclooxygenase 1 over cyclooxygenase 2 in the generation of proinflammatory prostaglandins in autoantibody-driven K/BxN serum-transfer arthritis. Arthritis Rheum. 2008;58:1354–1365
  8. Choe JY, Crain B, Wu SR, Corr M. Interleukin 1 receptor dependence of serum-transferred arthritis can be circumvented by toll-like receptor 4 signaling. J Exp Med. 2003;197:537–542
  9. Courtenay JS, Dallman MJ, Dayan AD, Martin A, Mosedale B. Immunisation against heterologous type II collagen induces arthritis in mice. Nature. 1980;283:666–668
  10. Coyle DE. Partial peripheral nerve injury leads to activation of astroglia and microglia which parallels the development of allodynic behavior. Glia. 1998;23:75–83
  11. Dhondt W, Willaeys T, Verbruggen LA, Oostendorp RA, Duquet W. Pain threshold in patients with rheumatoid arthritis and effect of manual oscillations. Scand J Rheumatol. 1999;28:88–93
  12. Dirig DM, Salami A, Rathbun ML, Ozaki GT, Yaksh TL. Characterization of variables defining hindpaw withdrawal latency evoked by radiant thermal stimuli. J Neurosci Methods. 1997;76:183–191
  13. Domer F. Characterization of the analgesic activity of ketorolac in mice. Eur J Pharmacol. 1990;177:127–135
  14. Edwards RR, Wasan AD, Bingham CO, Bathon J, Haythornthwaite JA, Smith MT, et al. Enhanced reactivity to pain in patients with rheumatoid arthritis. Arthritis Res Ther. 2009;11:R61
  15. Eroglu C, Allen NJ, Susman MW, O’Rourke NA, Park CY, Ozkan E, et al. Gabapentin receptor alpha2delta-1 is a neuronal thrombospondin receptor responsible for excitatory CNS synaptogenesis. Cell. 2009;139:380–392
  16. Fehrenbacher JC, Taylor CP, Vasko MR. Pregabalin and gabapentin reduce release of substance P and CGRP from rat spinal tissues only after inflammation or activation of protein kinase C. Pain. 2003;105:133–141
  17. Garrison CJ, Dougherty PM, Kajander KC, Carlton SM. Staining of glial fibrillary acidic protein (GFAP) in lumbar spinal cord increases following a sciatic nerve constriction injury. Brain Res. 1991;565:1–7
  18. Geranton SM, Jimenez-Diaz L, Torsney C, Tochiki KK, Stuart SA, Leith JL, et al. A rapamycin-sensitive signaling pathway is essential for the full expression of persistent pain states. J Neurosci. 2009;29:15017–15027
  19. Gerecz-Simon EM, Tunks ER, Heale JA, Kean WF, Buchanan WW. Measurement of pain threshold in patients with rheumatoid arthritis, osteoarthritis, ankylosing spondylitis, and healthy controls. Clin Rheumatol. 1989;8:467–474
  20. Hai T, Wolfgang CD, Marsee DK, Allen AE, Sivaprasad U. ATF3 and stress responses. Gene Exp. 1999;7:321–335
  21. Hamann W, Abou-Sherif S, Thompson S, Hall S. Pulsed radiofrequency applied to dorsal root ganglia causes a selective increase in ATF3 in small neurons. Eur J Pain. 2006;10:171–176
  22. Herrero JF, Laird JM, Lopez-Garcia JA. Wind-up of spinal cord neurones and pain sensation: much ado about something?. Prog Neurobiol. 2000;61:169–203
  23. Hua XY, Svensson CI, Matsui T, Fitzsimmons B, Yaksh TL, Webb M. Intrathecal minocycline attenuates peripheral inflammation-induced hyperalgesia by inhibiting p38 MAPK in spinal microglia. Eur J Neurosci. 2005;22:2431–2440
  24. Inglis JJ, Notley CA, Essex D, Wilson AW, Feldmann M, Anand P, et al. Collagen-induced arthritis as a model of hyperalgesia: functional and cellular analysis of the analgesic actions of tumor necrosis factor blockade. Arthritis Rheum. 2007;56:4015–4023
  25. Inglis JJ, Simelyte E, McCann FE, Criado G, Williams RO. Protocol for the induction of arthritis in C57BL/6 mice. Nat Protoc. 2008;3:612–618
  26. Inoue K, Tsuda M. Microglia and neuropathic pain. Glia. 2009;57:1469–1479
  27. Ivanavicius SP, Ball AD, Heapy CG, Westwood FR, Murray F, Read SJ. Structural pathology in a rodent model of osteoarthritis is associated with neuropathic pain: increased expression of ATF-3 and pharmacological characterisation. Pain. 2007;128:272–282
  28. Ji H, Pettit A, Ohmura K, Ortiz-Lopez A, Duchatelle V, Degott C, et al. Critical roles for interleukin 1 and tumor necrosis factor alpha in antibody-induced arthritis. J Exp Med. 2002;196:77–85
  29. Jin X, Gereau RWt. Acute p38-mediated modulation of tetrodotoxin-resistant sodium channels in mouse sensory neurons by tumor necrosis factor-alpha. J Neurosci. 2006;26:246–255
  30. Jones E, Vinuela-Fernandez I, Eager RA, Delaney A, Anderson H, Patel A, et al. Neuropathic changes in equine laminitis pain. Pain. 2007;132:321–331
  31. Kidd BL, Photiou A, Inglis JJ. The role of inflammatory mediators on nociception and pain in arthritis. Novartis Found Symp. 2004;260:122–133[discussion 133–128, 277–129]
  32. Knight B, Katz DR, Isenberg DA, Ibrahim MA, Le Page S, Hutchings P, et al. Induction of adjuvant arthritis in mice. Clin Exp Immunol. 1992;90:459–465
  33. Kouskoff V, Korganow AS, Duchatelle V, Degott C, Benoist C, Mathis D. Organ-specific disease provoked by systemic autoimmunity. Cell. 1996;87:811–822
  34. Leffler AS, Kosek E, Lerndal T, Nordmark B, Hansson P. Somatosensory perception and function of diffuse noxious inhibitory controls (DNIC) in patients suffering from rheumatoid arthritis. Eur J Pain. 2002;6:161–176
  35. Li MM, Yu YQ, Fu H, Xie F, Xu LX, Chen J. Extracellular signal-regulated kinases mediate melittin-induced hypersensitivity of spinal neurons to chemical and thermal but not mechanical stimuli. Brain Res Bull. 2008;77:227–232
  36. Lu Y, Westlund KN. Gabapentin attenuates nociceptive behaviors in an acute arthritis model in rats. J Pharmacol Exp Ther. 1999;290:214–219
  37. Malfait AM, Ritchie J, Gil AS, Austin JS, Hartke J, Qin W, et al. ADAMTS-5 deficient mice do not develop mechanical allodynia associated with osteoarthritis following medial meniscal destabilization. Osteoarthritis Cartil. 2010;18:572–580
  38. Maneuf YP, Hughes J, McKnight AT. Gabapentin inhibits the substance P-facilitated K(+)-evoked release of [(3)H]glutamate from rat caudial trigeminal nucleus slices. Pain. 2001;93:191–196
  39. Matsumoto I, Staub A, Benoist C, Mathis D. Arthritis provoked by linked T and B cell recognition of a glycolytic enzyme. Science. 1999;286:1732–1735
  40. McMahon SB, Malcangio M. Current challenges in glia-pain biology. Neuron. 2009;64:46–54
  41. Milligan ED, O’Connor KA, Armstrong CB, Hansen MK, Martin D, Tracey KJ, et al. Systemic administration of CNI-1493, a p38 mitogen-activated protein kinase inhibitor, blocks intrathecal human immunodeficiency virus-1 gp120-induced enhanced pain states in rats. J Pain. 2001;2:326–333
  42. Monach PA, Mathis D, Benoist C. The K/BxN arthritis model. Curr Protoc Immunol 2008 [Chapter 15 and Unit 15–22].
  43. Nozaki-Taguchi N, Yaksh TL. A novel model of primary and secondary hyperalgesia after mild thermal injury in the rat. Neurosci Lett. 1998;254:25–28
  44. 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
  45. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29:e45
  46. Raghavendra V, Tanga FY, DeLeo JA. Complete Freunds adjuvant-induced peripheral inflammation evokes glial activation and proinflammatory cytokine expression in the CNS. Eur J Neurosci. 2004;20:467–473
  47. Romero-Sandoval A, Chai N, Nutile-McMenemy N, Deleo JA. A comparison of spinal Iba1 and GFAP expression in rodent models of acute and chronic pain. Brain Res. 2008;1219:116–126
  48. Rosner H, Rubin L, Kestenbaum A. Gabapentin adjunctive therapy in neuropathic pain states. Clin J Pain. 1996;12:56–58
  49. Schaible HG, Richter F, Ebersberger A, Boettger MK, Vanegas H, Natura G, et al. Joint pain. Exp Brain Res. 2009;196:153–162
  50. Schwei MJ, Honore P, Rogers SD, Salak-Johnson JL, Finke MP, Ramnaraine ML, et al. Neurochemical and cellular reorganization of the spinal cord in a murine model of bone cancer pain. J Neurosci. 1999;19:10886–10897
  51. Segal AZ, Rordorf G. Gabapentin as a novel treatment for postherpetic neuralgia. Neurology. 1996;46:1175–1176
  52. Sokka T, Kautiainen H, Toloza S, Makinen H, Verstappen SM, Lund Hetland M, et al. QUEST-RA: quantitative clinical assessment of patients with rheumatoid arthritis seen in standard rheumatology care in 15 countries. Ann Rheum Dis. 2007;66:1491–1496
  53. Svensson CI, Brodin E. Spinal astrocytes in pain processing: non-neuronal cells as therapeutic targets. Mol Interv. 2010;10:25–38
  54. Sweitzer SM, Colburn RW, Rutkowski M, DeLeo JA. Acute peripheral inflammation induces moderate glial activation and spinal IL-1beta expression that correlates with pain behavior in the rat. Brain Res. 1999;829:209–221
  55. Sweitzer SM, Schubert P, DeLeo JA. Propentofylline, a glial modulating agent, exhibits antiallodynic properties in a rat model of neuropathic pain. J Pharmacol Exp Ther. 2001;297:1210–1217
  56. Takasu K, Honda M, Ono H, Tanabe M. Spinal alpha(2)-adrenergic and muscarinic receptors and the NO release cascade mediate supraspinally produced effectiveness of gabapentin at decreasing mechanical hypersensitivity in mice after partial nerve injury. Brit J Pharmacol. 2006;148:233–244
  57. Tanabe M, Ono K, Honda M, Ono H. Gabapentin and pregabalin ameliorate mechanical hypersensitivity after spinal cord injury in mice. Eur J Pharmacol. 2009;609:65–68
  58. Thompson SW, Dray A, Urban L. Leukemia inhibitory factor induces mechanical allodynia but not thermal hyperalgesia in the juvenile rat. Neuroscience. 1996;71:1091–1094
  59. Tsuda M, Shigemoto-Mogami Y, Koizumi S, Mizokoshi A, Kohsaka S, Salter MW, et al. P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature. 2003;424:778–783
  60. 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
  61. Tsuzuki K, Kondo E, Fukuoka T, Yi D, Tsujino 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
  62. Villanueva L, Chitour D, Le Bars D. Involvement of the dorsolateral funiculus in the descending spinal projections responsible for diffuse noxious inhibitory controls in the rat. J Neurophysiol. 1986;56:1185–1195
  63. Watkins LR, Martin D, Ulrich P, Tracey KJ, Maier SF. Evidence for the involvement of spinal cord glia in subcutaneous formalin induced hyperalgesia in the rat. Pain. 1997;71:225–235
  64. Wipke BT, Wang Z, Kim J, McCarthy TJ, Allen PM. Dynamic visualization of a joint-specific autoimmune response through positron emission tomography. Nat Immunol. 2002;3:366–372
  65. Zimmermann M. Pathobiology of neuropathic pain. Eur J Pharmacol. 2001;429:23–37

PII: S0304-3959(10)00452-5

doi: 10.1016/j.pain.2010.07.030

PAIN
Volume 151, Issue 2 , Pages 394-403 , November 2010