Focal peripheral nerve injury induces leukocyte trafficking into the central nervous system: Potential relationship to neuropathic pain

Pain

Volumn 100, Issue 1-2, 2002, Pages 163-170

  Sweitzer, Sarah M ^a   Hickey, William F ^a   Rutkowski, Maria D ^b   Pahl, Janice L ^b   DeLeo, Joyce A ^b  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b DARTMOUTH HITCHCOCK MEDICAL CENTER   (United States)

Author keywords

Macrophage; Major histocompatibility complex; Neuropathic pain; T lymphocyte

Indexed keywords

CD3 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1;

ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; CELL STRUCTURE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CORRELATION ANALYSIS; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; IRRADIATION; LYMPHOCYTIC INFILTRATION; MACROPHAGE; MALE; NEUROPATHIC PAIN; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; RAT; SPINAL CORD; T LYMPHOCYTE;

ANIMALS; CELL MOVEMENT; DENERVATION; HISTOCOMPATIBILITY ANTIGENS CLASS I; MACROPHAGES; MALE; NEURALGIA; NEUROIMMUNOMODULATION; RADIATION CHIMERA; RADICULOPATHY; RATS; RATS, INBRED BN; RATS, INBRED LEW; RATS, SPRAGUE-DAWLEY; SPINAL CORD; SPINAL NERVES; T-LYMPHOCYTES;

EID: 0036844372     PISSN: 03043959     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0304-3959(02)00257-9     Document Type: Article

References (64)

1. Aley K., McCarter G., Levine J. Nitric oxide signaling in pain and nociceptor sensitization in the rat. J Neurosci. 18:1998;7008-7014.
2. Arruda J.L., Sweitzer S., Rukowski M.D., DeLeo J.A. Intrathecal anti-IL-6 antibody and IgG attenuates peripheral nerve injury-induced mechanical allodynia in the rat: possible immune modulation in neuropathic pain. Brain Res. 879:2000;216-225.
3. Aschner M. Astrocytes as mediators of immune and inflammatory responses in the CNS. Neurotoxicology. 19:1998;269-280.
4. Bauer J., Huitinga I., Zhao W., Lassman H., Hickey W.F., Dijkstra C.D. The role of macrophages, perivascular cells, and microglial cells in the pathogenesis of experimental autoimmune encephalomyelitis. Glia. 15:1995;437-446.
5. Bechmann I., Peter S., Beyer M., Gimsa U., Nitsch R. Presence of B-7.2 (CD86) and lack of B7-1 (CD80) on myelin-phagocytosing MHC-II positive rat microglia are associated with nondestructive immunity in vivo. FASEB. 15:2001;1086-1088.
6. Belyantseva I.A., Lewin G.R. Stability and plasticity of primary afferent projections following nerve regeneration and central degeneration. Eur J Neurosci. 11:1999;457-468.
7. Boddeke E.W.G.M. Involvement of chemokines in pain. Eur J Pharmacol. 429:2001;115-119.
8. Brazelton T., Rossi F., Keshet G., Blau H. From marrow to brain: expression of neuronal phenotypes in adult mice. Science. 290:2000;1775-1779.
9. Colburn R.W., DeLeo J.A., Rickman A.J., Yeager M., Kwon P., Hickey W.F. Dissociation of microglial activation and neuropathic pain behaviors following peripheral nerve injury in the rat. J Neuroimmunol. 79:1997;163-175.
10. Coyle D. Partial peripheral nerve injury leads to activation of astroglia and microglia which parallel the development of allodynic behavior. Glia. 23:1998;75-83.
11. Cui J.-G., Holmin S., Mathiesen T., Meyerson B., Linderoth B. Possible role of inflammatory mediators in tactile hypersensitivity in rat models of mononeuropathy. Pain. 88:2000;239-248.
12. DeLeo J.A., Colburn R.W. The role of cytokines in nociception and chronic pain. Weinstein J., Gordon S., Low back pain: a scientific and clinical overview. 1996;163-185 American Academy of Orthopaedic Surgeons, Rosemont, IL.
13. DeLeo J.A., Colburn R.W. Proinflammatory cytokines and glial cells: their role in neuropathic pain. Watkins L., Maier S., Cytokines and pain: progress in inflammation research. 1999;159-181 Birkhauser Verlag, Basel.
14. DeLeo J., Yezierski R. The role of neuroinflammation and neuroimmune activation in persistent pain. Pain. 90:2001;1-6.
15. Eliav E., Herzberg U., Ruda M., Bennett G.J. Neuropathic pain from an experimental neuritis of the rat sciatic nerve. Pain. 83:1999;169-182.
16. Fine S., Angel R., Perry S., Epstein L., Rothstein J., Dewhurst S., Gelbard H. Tumor necrosis factor alpha inhibits glutamate uptake by primary human astrocytes. J Biochem. 271:1996;15303-15306.
17. Garrison C., Dougherty P., Kajander K., Carlton S. Staining of glial fibrillary acidic protein (GFAP) in lumbar spinal cord increases following a sciatic nerve constriction injury. Brain Res. 565:1991;1-7.
18. Garrison C., Dougherty P., Carlton S. GFAP expression in lumbar spinal cord of naive and neuropathic rats treated with MK-801. Exp Neurol. 129:1994;237-243.
19. Grusby M.J., Glimcher L.H. Immune responses in MHC class II-deficient mice. Annu Rev Immunol. 13:1995;417-435.
20. Grusby M.J., Johnson R.S., Papaioannaou V.E., Glimcher L.H. Depletion of CD4+ T cells in major histocompatibility complex II-deficient mice. Science. 253:1991;1417-1420.
21. Hart M., Fabry Z. CNS antigen presentation. Trends Neurosci. 18:1995;475-481.
22. Hashizume H., DeLeo J.A., Colburn R.W., Weinstein J.N. Spinal glial activation and cytokine expression after lumbar root injury in the rat. Spine. 25:2000;1206-1217.
23. Hashizume H., Rutkowski M., Weinstein J., DeLeo J. Central administration of methotrexate reduces mechanical allodynia in an animal model of radiculopathy/sciatica. Pain. 87:2000;159-169.
24. Hickey W., Kimura H. Perivascular microglia are bone marrow derived and present antigen in vivo. Science. 239:1988;290-292.
25. Hickey W.F., Vass K., Lassmann H. Bone marrow derived elements in the central nervous system: an immunohistochemical and ultrastructural survey of rat chimeras. J Neuropathol Exp Neurol. 51:1992;246-256.
26. Hohlfeld R., Kershensteiner M., Stadelmann C., Lassmann H., Wekerle H. The neuroprotective effect of inflammation: implications for the therapy of multiple sclerosis. J Neuroimmunol. 107:2000;161-166.
27. Huh G., Boulanger L., Du H., Riquelme P., Brotz T., Shatz C. Functional requirement for class I MHC in CNS development and plasticity. Science. 290:2000;2155-2159.
28. Inoue A., Ikoma K., Morioka N., Kumagia K., Hashimoto T., Hilde I., Nakata Y. Interleukin-1β induces substance P release from primary afferent neurons through the cyclooxygenase-2 system. J Neurochem. 73:1999;2206-2213.
29. Jeanjean A., Moussaoui S., Maloteaux J., Laduron P. Interleukin-1β induces long term increase of axonally transported opiate receptors and substance P. Neuroscience. 68:1995;151-157.
30. Koller H., Thiem K., Siebler M. Tumour necrosis factor-alpha increases intracellular Ca2+ and induces a depolarization in cultured astroglial cells. Brain. 119:1996;2021-2027.
31. Kreutzberg G. Microglia: a sensor of pathological events in the CNS. Trends Neurosci. 19:1996;312-318.
32. Malcangio M., Bowery N., Flower R., Perretti M. Effect of interleukin-1 beta on the release of substance P from rat isolated spinal cord. Eur J Pharmacol. 299:1996;113-118.
33. Mallat M., Chamak B. Brain macrophages: neurotoxic or neurotrophic effector cells? J Leukoc Biol. 56:1994;416-422.
34. McCluskey L.P., Lampson L.A. Local immune regulation in the central nervous system by substance P vs. glutamate. J Neuroimmunol. 116:2001;136-146.
35. Meller S., Dykstra C., Grzybycki D., Murphy S., Gebhart G. The possible role of glia in nociceptive processing and hyperalgesia in the spinal cord of the rat. Neuropharmacology. 33:1994;1471-1478.
36. Mezey E., Chandross K., Harta G., Maki R., McKercher S. Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow. Science. 290:2000;1779-1782.
37. Milligan E.D., O'Connor K.A., Nguyen K.T., Armstrong C.B., Twining C., Gaykema R.P., Holguin A., Martin D., Maier S.F., Watkins L.R. Intrathecal HIV-1 envelope glycoprotein gp120 induces enhanced pain states mediated by spinal proinflammatory cytokines. J Neurosci. 21:2001;2808-2819.
38. Nicol G., Lopshire J., Pafford C. Tumor necrosis factor enhances the capsaicin sensitivity of rat sensory neurons. J Neurol. 17:1997;975-982.
39. Palma C., Minghett L., Astolfi M., Ambrosini E., Silberstein F., Manzini S., Levi G., Aloisi F. Functional characterization of substance P receptors on cultured human spinal cord astrocytes: synergism of substance P with cytokines in inducing interleukin-6 and prostaglandin E2 production. Glia. 21:1997;183-193.
40. Perkins M., Tracey D. Hyperalgesia due to nerve injury: role of neutrophils. Neuroscience. 101:2000;745-757.
41. Popovich P., Streit W., Stokes B. Differential expression of MHC class II antigen in the contused rat spinal cord. J Neurotrauma. 10:1993;37-46.
42. Raivich G., Bohatschek M., Kloss C., Werner A., Jones L., Kreutzberg G. Neuroglial activation repertoire in the injured brain: graded response, molecular mechanisms and cues to physiological function. Brain Res Rev. 30:1999;77-105.
43. Ribeiro R.A., Vale M.L., Ferreira S.H., Cunha F.Q. Analgesic effect of thalidomide on inflammatory pain. Eur J Pharmacol. 391:2000;97-103.
44. Ruffolo R., Fuerstein G.Z., Hunter A.J., Poste G., Metcalf B.W. Inflammatory cells and mediators in CNS disease. 1999;Harwood Academic, Netherlands.
45. Rutkowski M.D., Arruda J., Sweitzer S., DeLeo J.A. The limited role of peripheral macrophages in the generation of neuropathic pain behavior in a rat model of neuropathy. Physiol Behav. 71:2000;225-235.
46. Schnell L., Fearn S., Klassen H., Schwab M., Perry V. Acute inflammatory responses to mechanical lesions in the CNS: differences between brain and spinal cord. Eur J Neurosci. 11:1999;3648-3658.
47. Schwartz M., Moalem G., Leibowitz-Amit R., Cohen I.R. Innate and adaptive immune responses can be beneficial for CNS repair. Trends Neurosci. 22:1999;295-299.
48. Seabrook T., Hay J. Intracerebroventricular infusions of TNF-α preferentially recruit blood lymphocytes and induce a perivascular leukocyte infiltrate. J Neuroimmunol. 113:2001;81-88.
49. Shrikant P., Benveniste E. The central nervous system as an immunocompetent organ. Role of glial cells in antigen presentation. J Immunol. 157:1996;1819-1822.
50. Sommer C., Marziniak M., Myers R. The effect of thalidomide treatment on vascular pathology and hyperalgesia caused by chronic constriction injury of rat nerve. Pain. 74:1998;83-91.
51. Streit W., Graeber M., Kreutzberg G. Peripheral nerve lesion produces increased levels of major histocompatibility complex antigens in the central nervous system. J Neuroimmunol. 21:1989;117-123.
52. Sweitzer S., Colburn R.W., Rukowski M., DeLeo J.A. Acute peripheral inflammation induces moderate glial activation and spinal IL-1β expression that correlates with pain behavior in the rat. Brain Res. 829:1999;209-221.
53. Sweitzer S., Schubert P., DeLeo J.A. Propentofylline, a glial modulating agent, exhibits anti-allodynic properties in a rat model of neuropathic pain. J Pharmacol Exp Ther. 297:2001;1210-1217.
54. Sweitzer S., Martin D., DeLeo J.A. Intrathecal interleukin-1 receptor antagonist in combination with soluble tumor necrosis factor receptor exhibit an anti-allodynic action in a rat model of neuropathic pain. Neuroscience. 103:2001;529-539.
55. Sweitzer SM, DeLeo JA. The active metabolite of leflunomide, an immunosuppressive agent, reduces mechanical sensitivity in a rat mononeuropathy model. J Pain 2002 (in press).
56. Sweitzer S.M., White K.A., Dutta C., DeLeo J.A. The differential role of spinal MHC class II and cellular adhesion molecules in inflammatory versus neuropathic pain in rodents. J Neuroimmunol. 125:2002;82-93.
57. Vass K., Lassmann H. Intrathecal application of interferon gamma. Progressive appearance of MHC antigens within the rat nervous system. Am J Pathol. 137:1990;789-800.
58. Watkins L., Maier S., Goehler L. Immune activation: the role of pro-inflammatory cytokines in inflammation, illness responses and pathological pain states. Pain. 63:1995;289-302.
59. Watkins L., Martin D., Ulrich P., Tracey K., Maier S. Evidence for the involvement of spinal cord glia in subcutaneous formalin induced hyperalgesia in the rat. Pain. 71:1997;225-235.
60. Watkins L.R., Milligan E.D., Maier S.F. Glial activation: a driving force for pathological pain. Trends Neurosci. 24:2001;450-455.
61. Wilson P., Kitchener P.D. Plasticity of cutaneous primary afferent projections to the spinal dorsal horn. Prog Neurobiol. 48:1996;105-129.
62. Winkelstein B.A., Rutkowski M.D., Sweitzer S.M., Pahl J.L., DeLeo J.A. Nerve injury proximal or distal to the DRG induces similar spinal glial activation and selective cytokine expression but differential behavioral responses to pharmacological treatment. J Comp Neurol. 439:2001;127-139.
63. Woolf C.J., Shortland P., Reynolds M., Ridings J., Doubell T., Coggeshall R.E. Reorganization of central terminals of myelinated primary afferents in the rat dorsal horn following peripheral axotomy. J Comp Neurol. 360:1995;121-134.
64. Woolf C.J., Shortland P., Coggeshall R.E. Peripheral nerve injury triggers central sprouting of myelinated afferents. Nature. 355:1992;75-78.