Cytokine antagonism reduces pain and modulates spinal astrocytic reactivity after cervical nerve root compression

Annals of Biomedical Engineering

Volumn 38, Issue 8, 2010, Pages 2563-2576

  Rothman, Sarah M ^a   Winkelstein, Beth A ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Astrocytes; Compression; Cytokine; Nerve root; Pain; Radiculopathy

Indexed keywords

CYTOKINES; DIFFERENTIAL EFFECT; NERVE ROOT COMPRESSION; RADICULOPATHY; RECEPTOR ANTAGONISTS; REDUCED SENSITIVITY; TIME POINTS;

HEALTH;

CYTOKINE; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1BETA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL; ARTICLE; ASTROCYTE; DRUG ANTAGONISM; GLIA; MALE; METABOLISM; NECK INJURY; PAIN; PATHOPHYSIOLOGY; RADICULOPATHY; RAT; SPINAL CORD COMPRESSION; SPRAGUE DAWLEY RAT;

ANIMALS; ASTROCYTES; CYTOKINES; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; INTERLEUKIN-1; INTERLEUKIN-1BETA; MALE; NECK INJURIES; NEUROGLIA; PAIN; RADICULOPATHY; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD COMPRESSION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 77955174911     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-010-0012-8     Document Type: Article

References (59)

1. Aloisi, F. Immune function of microglia. Glia 36:165-179, 2001.
2. Atlas, S., R. Keller, Y. Wu, R. Deyo, and D. Singer. Longterm outcomes of surgical and nonsurgical management of sciatica secondary to a lumbar disc herniation: 10 year results from the maine lumbar spine study. Spine 30:927-935, 2005. (Pubitemid 40632539)
3. Binshtok, A., H. Wang, K. Zimmermann, F. Amaya, D. Vardeh, L. Shi, G. Brenner, R. Ji, B. Bean, C. Woolf, and T. Samad. Nociceptors are interleukin-1 beta sensors. J. Neurosci. 28:14062-14073, 2008.
4. Colburn, R. W., A. J. Rickman, and J. A. DeLeo. The effect of site and type of nerve injury on spinal glial activation and neuropathic pain behavior. Exp. Neurol. 157:289-304, 1999.
5. Davies, A. L., K. C. Hayes, and G. A. Dekaban. Clinical correlates of elevated serum concentrations of cytokines and autoantibodies in patients with spinal cord injury. Arch. Phys. Med. Rehabil. 88:1384-1393, 2007.
6. DeLeo, J. A., R. W. Colburn, M. Nichols, and A. Malhotra. Interleukin-6-mediated hyperalgesia/allodynia and increased spinal IL-6 expression in a rat mononeuropathy model. J. Interferon Cytokine Res. 16:695-700, 1996.
7. DeLeo, J. A., and R. P. Yezierski. The role of neuroinflammation and neuroimmune activation in persistent pain. Pain 90:1-6, 2001.
8. Dinarello, C. A. IL-1α. In: Cytokine Reference, edited by J. J. Oppenheim and M. Feldman. New York: Academic Press, 2001, pp. 307-318.
9. Dinarello, C. A. IL-1β. In: Cytokine Reference, edited by J. J. Oppenheim and M. Feldman. New York: Academic Press, 2001, pp. 351-374.
10. Eskes, C., L. Juillerat-Jeanneret, G. Leuba, P. Honegger, and F. Monnet-Tschudi. Involvement of microglia-neuron interactions in the tumor necrosis factor release, microglial activation, and neurodegeneration induced by trimethyltin. J. Neurosci. Res. 71:583-590, 2003.
11. Frymoyer, J. Back pain and sciatica. NEJM 318:291-300, 1988.
12. Goldenberg, M. Etanercept, a novel drug for the treatment of patients with severe, active rheumatoid arthritis. Clin. Ther. 21:75-87, 1999.
13. Hanisch, U. Microglia as a source and target of cytokines. Glia 40:140-155, 2002.
14. Hart, L., R. Deyo, and D. Cherkin. Physician office visits for low back pain. Frequency, clinical evaluation, and treatment patterns from a U.S. national survey. Spine 20:11-19, 1995.
15. Hashizume, H., J. A. DeLeo, R. W. Colburn, and J. N. Weinstein. Spinal glial activation and cytokine expression after lumbar root injury in the rat. Spine 25:1206-1217, 2000.
16. Homma, Y., S. J. Brull, and J. M. Zhang. A comparison of chronic pain behavior following local application of tumor necrosis factor a to the normal and mechanically compressed lumbar ganglia in the rat. Pain 95:239-246, 2002.
17. Hubbard, R. D., Z. Chen, and B. A. Winkelstein. Transient cervical nerve root compression modulates pain: load thresholds for allodynia and sustained changes in spinal neuropeptide expression. J. Biomech. 41:677-685, 2008.
18. Hubbard, R. D., J. J. Martinez, J. A. Burdick, and B. A. Winkelstein. Controlled release of GDNF reduces nerve root-mediated behavioral hypersensitivity. J. Orthop. Res. 27:120-127, 2009.
19. Hubbard, R. D., 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 30:1924-1932, 2005.
20. Ji, R., T. Kohno, K. Moore, and C. Woolf. Central sensitization and LTP: do pain and memory share similar mechanisms? Trends Neurosci. 26:696-705, 2003.
21. Kawasaki, Y., L. Zhang, J. Cheng, and R. Ji. Cytokine mechanisms of central sensitization: Distinct and overlapping role of interleukin-1 beta, interleukin-6, and tumor necrosis factor-alpha in regulating synaptic and neuronal activity in the superficial spinal cord. J. Neurosci. 28:5189-5194, 2008.
22. Lee, D., S. Iyengar, and D. Lodge. The role of uninjured nerve in spinal nerve ligated rats points to an improved animal model of neuropathic pain. Eur. J. Pain 7:473-479, 2003.
23. Lee, S., W. Liu, D. Dickson, C. Brosnan, and J. Berman. Cytokine production by human fetal microglia and astrocytes. Differential induction by lipopolysaccharide and IL-1beta. J. Immunol. 150:2659-2667, 1993.
24. Lindenlaub, T., P. Teuteberg, T. Hartung, and C. Sommer. Effects of neutralizing antibodies to TNF-alpha on painrelated behavior and nerve regeneration in mice with chronic constriction injury. Brain Res. 866:15-22, 2000.
25. Matsubayashi, T., H. Sugiura, T. Arai, T. Oh-Ishi, and Y. Inamo. Anakinra therapy for CINCA syndrome with a novel mutation in exon 4 of the CIAS1 gene. Acta Paediatr. 95:246-249, 2005.
26. McMahon, S. B., W. B. Cafferty, and F. Marchand. Immune and glial cell factors as pain mediators and modulators. Exp. Neurol. 192:444-462, 2005.
27. Mika, J., M. Korostynski, D. Kaminska, A. Wawrzczak- Bargiela, M. Osikowicz, W. Makuch, R. Przewlocki, and B. Przewlocka. Interleukin-1alpha has antiallodynic and antihyperalgesic activities in a rat neuropathic pain model. Pain 138:587-597, 2008.
28. Murata, Y., K. Olmarker, I. Takahashi, K. Takahashi, and B. Rydevik. Effects of selective tumor necrosis factor-alpha inhibition to pain-behavioral changes caused by nucleus pulposus-induced damage to the spinal nerve in rats. Neurosci. Lett. 382:148-152, 2005.
29. Newman, E. New roles for astrocytes: regulation of synaptic transmission. Trends Neurosci. 26:536-542, 2003.
30. Norimoto, M., S. Ohtori, M. Yamashita, G. Inoue, K. Yamauchi, T. Koshi, M. Suzuki, S. Orita, Y. Eguchi, A. Sugiura, N. Ochiai, M. Takaso, and K. Takahashi. Direct application of the TNF-alpha inhibitor, etanercept, does not affect CGRP expression and phenotypic change of DRG neurons following application of nucleus pulposus onto injured sciatic nerves in rats. Spine 33:2403-2408, 2008.
31. Ohnmeiss, D., H. Vanharanta, and J. Ekholm. Degree of disc disruption and lower extremity pain. Spine 22:1600-1605, 1997.
32. Ohtori, S., K. Takahashi, H. Moriya, and R. Myers. TNFalpha and TNF-alpha receptor type 1 upregulation in glia and neurons after peripheral nerve injury: studies in murine DRG and spinal cord. Spine 29:1082-1088, 2004.
33. Olmarker, K., and R. Myers. Pathogenesis of sciatic pain: role of herniated nucleus pulposus and deformation of spinal nerve root and dorsal root ganglion. Pain 78:99-105, 1998.
34. Ozaktay, A., S. Kallakuri, T. Takebayashi, J. Cavanaugh, I. Asik, J. A. DeLeo, and J. N. Weinstein. Effects of interleukin-1 beta, interleukin-6, and tumor necrosis factor on sensitivity of dorsal root ganglion and peripheral receptive fields in rats. Eur. Spine J. 15:1529-1537, 2006.
35. Rhyu, K. W., A. J. Walsh, C. W. O'Neill, D. S. Bradford, and J. C. Lotz. The short-term effects of electrosurgical ablation on proinflammatory mediator production by intervertebral disc cells in tissue culture. Spine J. 7:451-458, 2007.
36. Robinson, I., and T. Meert. Stability of neuropathic pain symptoms in partial sciatic nerve ligation in rats is affected by suture material. Neurosci. Lett. 373:125-129, 2005.
37. Rohl, C., E. Armbrust, K. Kolbe, R. Lucius, E. Maser, S. Venz, and M. Gulden. Activated microglia modulate astroglial enzymes involved in oxidative and inflammatory stress and increase the resistance of astrocytes to oxidative stress in vitro. Glia 56:1114-1126, 2008.
38. Rothman, S. M., B. B. Guarino, and B. A. Winkelstein. Spinal microglial proliferation is evident in a rat model of painful disc herniation both in the presence of behavioral hypersensitivity and following minocycline treatment sufficient to attenuate allodynia. J. Neurosci. Res. 87(12): 2709-2717, 2009.
39. Rothman, S. M., Z. Huang, K. E. Lee, C. L. Weisshaar, and B. A. Winkelstein. Cytokine mRNA expression in painful radiculopathy. J. Pain 10:90-99, 2009.
40. Rothman, S. M., L. H. Ma, G. T. Whiteside, and B. A. Winkelstein. Inflammatory cytokine and chemokine expression in the dorsal root ganglion in a rat model of painful radiculopathy. Spine, 2010 (in press).
41. Rothman, S. M., and B. A. Winkelstein. Chemical and mechanical nerve root insults induce differential behavioral sensitivity and glial activation that are enhanced in combination. Brain Res. 1181:30-43, 2007.
42. Rydevik, B., M. Hasue, and P. Wehling. Etiology of sciatic pain and mechanisms of nerve root compression. In: The Lumbar Spine, edited by S. Wiesel, J. Weinsten, H. Herkowitz, J. Dvorak, and G. Bell. Philadelphia: WB Saunders Co., 1996, pp. 123-141.
43. Shamash, S., F. Reichert, and S. Rotshenker. The cytokine network of Wallerian degeneration: tumor necrosis factoralpha, interleukin-1alpha, and interleukin- 1beta. J. Neurosci. 22:3052-3060, 2002.
44. Shih, A., H. Fernandes, F. Choi, M. Kozoriz, Y. Liu, P. Li, C. Cowan, and A. Klegeris. Policing the police: astrocyte modulate microglial activation. J. Neurosci. 26:3887-3888, 2006.
45. Sommer, C., and M. Kress. Recent findings on how proinflammatory cytokines cause pain: peripheral mechanisms in inflammatory and neuropathic hyperalgesia. Neurosci. Lett. 361:184-187, 2004.
46. Sotgiu, M., M. Brambilla, M. Valente, and G. Biella. Contralateral input modulates the excitability of dorsal horn neurons involved in noxious signal processes. Potential role in neuronal sensitization. Somatosens. Mot. Res. 21:211-215, 2004.
47. Svensson, C. I., M. Schäfers, T. L. Jones, H. Powell, and L. S. Sorkin. Spinal blockade of TNF blocks spinal nerve ligation-induced increases in spinal P-p38. Neurosci. Lett. 379:209-213, 2005.
48. Sweitzer, S. M., R. W. Colburn, M. D. Rutkowski, and J. A. DeLeo. Acute peripheral inflammation induces moderate glial activation and spinal IL-1b expression that correlates with pain behavior in the rat. Brain Res. 829:209-221, 1999.
49. Sweitzer, S. M., D. Martin, and J. A. DeLeo. Intrathecal interleukin-1 receptor antagonist in combination with soluble tumor necrosis factor receptor exhibits an antiallodynic action in a rat model of neuropathic pain. J. Neurosci. 103:529-539, 2001.
50. Taishi, P., L. Churchill, A. De, F. Obal, and J. Krueger. Cytokine mRNA induction by interleukin-1 beta or tumor necrosis factor alpha in vitro and in vivo. Brain Res. 1226:89-98, 2008.
51. Wall, P., and R. Melzak. Textbook of Pain, 3rd edn. London: Churchill Livingstone, 2005.
52. Watkins, L. R., S. F. Maier, and L. E. Goehler. Immune activation: the role of pro-inflammatory cytokines in inflammation, illness responses and pathological pain states. Pain 63:289-302, 1995.
53. Winkelstein, B. A. Mechanisms of central sensitization, neuroimmunology & injury biomechanics in persistent pain: implications for musculoskeletal disorders. Electromyogr. Kinesiol. 14:87-93, 2004.
54. Winkelstein, B. A., M. D. Rutkowski, S. M. Sweitzer, J. L. Pahl, and J. A. DeLeo. Nerve injury proximal or distal to the DRG induces similar spinal glial activation and selective cytokine expression but differential behavioral responses to pharmacologic treatment. J. Comp. Neurol. 439:127-139, 2001.
55. Woolf, C., and M. Salter. Neuronal plasticity: increasing the gain in pain. Science 288:1765-1768, 2000.
56. Wolf, G., R. Yirmiya, I. Goshen, K. Iverfeldt, L. Holmlund, K. Takeda, and Y. Shavit. Impairment of interleukin-1 (IL-1) signaling reduces basal pain sensitivity in mice: genetic, pharmacological and developmental aspects. Pain 104: 471-480, 2003.
57. Xu, J. T., W. J. Xin, Y. Zang, C. Y. Wu, and X. G. Liu. The role of tumor necrosis factor-alpha in the neuropathic pain induced by lumbar 5 ventral root transection in rat. Pain 123:306-321, 2006.
58. Zelenka, M., M. Schafers, and C. Sommer. Intraneural injection of interleukin-1-beta and tumor necrosis factoralpha into rat sciatic nerve at physiological doses induces signs of neuropathic pain. Pain 116:257-263, 2005.
59. Zimmermann, M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16:109-110, 1983.