Evidence that exogenous and endogenous fractalkine can induce spinal nociceptive facilitation in rats

European Journal of Neuroscience

Volumn 20, Issue 9, 2004, Pages 2294-2302

  Milligan, E D ^a   Zapata, V ^a,b   Chacur, M ^a,c   Schoeniger, D ^a   Biedenkapp, J ^a   O'Connor, K A ^a   Verge, G M ^d   Chapman, G ^e,f   Green, P ^e   Foster, A C ^d   Naeve, G S ^d,g   Maier, S F ^a   Watkins, L R ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSIDAD CENTRAL DE VENEZUELA   (Venezuela)

^c INSTITUTO BUTANTAN   (Brazil)

^d NEUROCRINE BIOSCIENCES INC   (United States)

^e GLAXOSMITHKLINE   (United Kingdom)

^f UCB PHARMA   (Belgium)

^g Parallax Biosystems Inc   (United States)

Author keywords

CX3CL1; CX3CR1; Mechanical allodynia; Microglia; Thermal hyperalgesia

Indexed keywords

CHEMOKINE; CX3C CHEMOKINE; FRACTALKINE; NEUTRALIZING ANTIBODY;

ALLODYNIA; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FACILITATION; GLIA CELL; HYPERALGESIA; MALE; NEUROIMMUNOLOGY; NEUROMODULATION; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; RAT; SENSITIZATION; SPINAL CORD NERVE CELL; THERMAL STIMULATION;

ANIMALS; ANTIBODIES; CELL COMMUNICATION; CHEMOKINES, CX3C; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; HYPERALGESIA; INJECTIONS, SPINAL; LIGATION; MALE; MEMBRANE PROTEINS; MICROGLIA; NEUROGLIA; NEURONS; NOCICEPTORS; PAIN; PERIPHERAL NERVOUS SYSTEM DISEASES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CYTOKINE; RECEPTORS, HIV; SCIATIC NEUROPATHY; SPINAL CORD;

EID: 8144221210     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2004.03709.x     Document Type: Article

References (53)

1. Abbadie, C., Lindia, J.A., Cumiskey, A.M., Peterson, L.B., Mudgett, J.S., Bayne, E.K., DeMartino, J.A., MacIntyre, D.E. & Forrest, M.J. (2003) Impaired neuropathic pain responses in mice lacking the chemokine receptor CCR2. Proc. Natl Acad. Sci. USA, 100, 7947-7952.
2. Aicher, S.A., Sharma, S., Cheng, P.Y. & Pickel, V.M. (1997) The N-methyl-D-aspartate (NMDA) receptor is postsynaptic to substance P-containing axon terminals in the rat superficial dorsal horn. Brain Res., 772, 71-81.
3. Arruda, J.L., Rutkowski, M.D., Sweitzer, S.M. & DeLeo, J.A. (2000) Antibody and IgG attenuate mechanical allodynia in a mononeuropathy model in the rat: potential role of immune modulation in neuropathic pain. Brain Res., 879, 216-225.
4. Asensio, V.C. & Campbell, I.L. (1999) Chemokines in the CNS: plurifunctional mediators in diverse states. Trends Neurosci., 22, 504-512.
5. Bennett, G.J. & Xie, Y.K. (1938) A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain, 33, 87-107.
6. Besong, G., Battaglia, G., D'Onofrio, M., DiMarco, R., Ngomba, R.T., Storto, M., Castiglione. M., Mangano, K., Busceti, C.L., Nicoletti, F.R., Bacon, K., Tusche, M., Valenti, O., Conn, P.J., Bruno, V. & Nicoletti, F. (2002) Activation of group III metabotropic glutamate receptors inhibits the production of RANTES in glial cell cultures. J. Neurosci., 22, 5403-5411.
7. Boddeke, E.W.G.M. (2001) Involvement of chemokines in pain. Eur. J. Pharmacol., 429, 115-119.
8. Chacur, M., Milligan, E.D., Gazda, L.S., Armstrong, C., Wang, H., Tracey, K.J., Maier, S.F. & Watkins, L.R. (2001) A new model of sciatic inflammatory neuritis (SIN): induction of unilateral and bilateral mechanical allodynia following acute unilateral peri-sciatic immune activation in rats. Pain, 94, 231-244.
9. Chaplan, S.R., Bach, F.W., Pogrel, J.W., Chung, J.M. & Yaksh, T.L. (1994) Quantitative assessment of tactile allodynia in the rat paw. J. Neurosci. Methods, 53, 55-63.
10. Chapman, G.A., Moores, K., Harrison, D., Campbell, C.A., Steward. B.R. & Strijbos, P.J.L.M. (2000) Fractalkine cleavage from neuronal membranes represents an acute event in the inflammatory response to excitotoxic brain damage. J. Neurosci., 20, RC87 (81-85).
11. Cross, A.K. & Woodroofe, M.N. (1999) Chemokine modulation of matrix metalloproteinase and TIMP production in adult rat brain microglia and a human microglial cell line in vitro. Glia, 28, 183-189.
12. Dailey, A.T., Avellino, A.M., Benthem, L., Silver, J. & Kliot, M. (1998) Complement depletion reduces macrophage infiltration and activation during Wallerian degeneration and axonal regeneration. J. Neurosci., 18, 6713-6722.
13. DeLeo, J.A., Tanga, F.Y. & Tawfik, V.L. (2004) Neuroimmune activation and neuroinflammation in chronic pain and opioid tolerance/hyperalgesia. Neuroscientist, 10, 40-52.
14. Erichsen, D., Lopez, A.L., Peng, H., Niemann, D., Williams, C., Bauer, M., Morgello, S., Cotter, R.L., Ryan, L.A., Ghorpade, A., Gendelman, H.E. & Zheng, J. (2003) Neuronal injury regulates fractalkine: relevance for HIV-1 associated dementia. J. Neuroimmunol., 138, 144-155.
15. Gazda, L.S., Milligan, E.D., Hansen, M.K., Twining, C.M., Paulos, N., Chacur, M., O'Connor, K.A., Armstrong, C. & Maier, S.F. (2001) Sciatic inflammatory neuritis (SIN): behavioral allodynia is paralleled by perisciatic proinflammatory cytokine and Superoxide production. J. Peripheral Nerv. Sys., 6, 111-129.
16. Hargreaves, K., Dubner, R., Brown, F., Flores, C. & Joris, J. (1998) A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain, 32, 77-88.
17. Harrison, J.K., Jiang, Y., Chen, S., Xia, Y., Maciejewski-Lenoir, D., McNamara, R.K., Streit, W.J., Salafranca, M.N., Adhikari, S., Thompson, D.A., Botti, P., Bacon, K..B. & Feng, L. (1998) Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proc. Natl Acad. Sci. USA, 95, 10896-10901.
18. Harvey, L.O.J. (1986) Efficient estimation of sensory thresholds. Behav. Res. Meth. Instrum. Comput., 18, 623-632.
19. Hecker-Kia, A., Kolkenbrock, H., Orgel, D., Zimmerman, B., Sparmann, M. & Ulbrich, N. (1997) Substance P induces the secretion of gelatinase A from human synovial fibroblasts. Eur. J. Clin. Chem. Biochem., 35, 655-660.
20. Honore, P. & Mantyh, P.W. (2000) Bone cancer pain: from mechanism to model to therapy. Pain Med., 1, 303-309.
21. Hughes, P.M., Batham, M.S., Frentzel, S., Mir, A. & Perry, V.H. (2002) Expression of fractalkine (CX3CL1) and its receptor (CX3CR1), during acute and chronic inflammation in the rodent CNS. Glia, 37, 314-327.
22. 3CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol. Cell. Biol., 20, 4106-4114.
23. Khalil, Z. & Khodr, B. (2001) A role for free radicals and nitric oxide in delayed recovery in aged rats with chronic constriction nerve injury. Free Radic. Biol. Med., 31, 430-439.
24. Lindenlaub, T., Teuteberg, P., Hartung, T. & Sommer, C. (2000) Effects of neutralizing antibodies to TNF-alpha on pain-related behavior and nerve regeneration in mice with chronic constriction injury. Brain Res., 866, 15-22.
25. Liu, T., Knight, K.R. & Racey, D.J. (2000) Hyperalgesia due to nerve injury - role of peroxynitrite. Neuroscience, 97, 125-131.
26. Lyons, C.A., Beharry, K.D., Nishihara, K.C., Akmal, Y., Ren, Z.Y., Chang, E. & Nageotte, M.P. (2002) Regulation of matrix metalloproteinases (type IV collagenases) and their inhibitors in the virgin, timed pregnant, and postpartum rat uterus and cervix by prostaglandin E(2)-cyclic adenosine monophosphate. Am. J. Obstet. Gynecol., 187, 202-208.
27. Marriott, D.R. & Wilkin, O.P. (1992) Preincubation with substance P induces substance P-stimulated phoshaidylinositol turnover in cultured cerebellar astrocytes. J. Neurochem., 59, 443-448.
28. Marriott, D.R., Wilkin, O.P., Coote, P.R. & Wood, J.N. (199Ia) Eicosanoid synthesis by spinal cord astrocytes is evoked by substance P. Adv. Prostaglandin Thromboxane Leukot. Res., 21B, 739-741.
29. Marriott, D.R., Wilkin, G.P. & Wood, J.N. (1991b) Substance P-induced release of prostaglandins from astrocytes: regional specalisation and correlation with phosphinositol metabolism. J. Neurochem., 56, 259-265.
30. Mayers, I., Hurst, T., Radomski, A., Johnson, D., Fricker, S., Bridger, G., Cameron, B., Darkes, M. & Radomski, M.W. (2003) Increased matrix metalloproteinase activity after canine cardiopulmonary bypass is suppressed by a nitric oxide scavenger. J. Thorac. Cardiovasc. Surg., 125. 661-668.
31. Medhurst, S.J., Walker, K., Bowes, M., Kidd, B.L., Glatt, M., Muller, M., Hattenberger, M., Vaxelaire, J., O'Reilly, T., Wotherspoon, G., Winter, J., Green, J. & Urban, L. (2002) A rat model of bone cancer pain. Pain, 96, 129-140.
32. Meller, S.T., Dyskstra, C., Grzybycki, D., Murphy, S. & Gebhart, G.F. (1994) The possible role of glia in nociceptive processing and hyperalgesia in the spinal cord of the rat. Neuropharmacology, 33, 1471-1478.
33. Milligan, E.D., Hinde, J.L., Mehmert, K.K., Maier, S.F. & Watkins, L.R. (1999) A method for increasing the viability of the external portion of the lumbar catheters placed in the spinal subarachnoid space of rats. J. Neurosci. Methods, 90, 81-86.
34. Milligan, E.D., Maier, S.F. & Watkins, L.R. (2004) Sciatic inflammatory neuropathy: A new model for studying neuropathic pain of inflammatory origin. In Luo, D. (Ed.), Pain Research Methods and Protocols: Methods of Molecular Medicine. Humana Press, New York, pp. 67-89
35. Milligan, E.D., Mehmert, K.K., Hinde, J.L., Harvey, L.O.J., Martin, D., Tracey, K.J., Maier, S.F. & Watkins, L.R. (2000) Thermal hyperalgesia and mechanical allodynia produced by intrathecal administration of the Human Immunodeficiency Virus-1 (HIV-1) envelope glycoprotein, gp120. Brain Res., 861, 105-116.
36. Milligan, E.D., O'Connor, K.A., Nguyen, K.T., Armstrong, C.B., Twining, C., Gaykema, R., Holguin, A., Martin, D., Maier, S.F. & Watkins, L.R. (2001) Intrathecal HIV-1 envelope glycoprotein gp120 enhanced pain states mediated by spinal cord proinflammatory cytokines. J. Neurosci., 21, 2808-2819.
37. Murphy, P.M. (2002) International union of pharmacology. XXX. Update on chemokine receptor nomenclature. Pharmacol. Rev., 54, 227-229.
38. Nagy, I., Woolf, C.J., Dray, A. & Urban, L. (1994) Cobalt accumulation in neurons expressing ionotropic excitatory amino acid receptors in young rat spinal cord: morphology and distribution. J. Comp. Neurol., 344, 321-335.
39. Palma, C., Minghetti, L., Astolfi, M., Ambrosini, E., Silberstein, F.C., Manzini, S., Levi, G. & Aloisi, F. (1997) 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, 183-193.
40. Paulson, P.E., Morrow, T.J. & Casey, K.L. (2000) Bilateral behavioral and regional cerebral blood flow changes during painful peripheral mononeuropathy in the rat. Pain, 84, 233-245.
41. Raghavendra, V., Tanga, F. & DeLeo, J.A. (2003) Inhibition, of microglial activation attenuates the development but not existing hypersensitivity in a rat model of neuropathy. J. Pharmacol. Exp. Ther., 306, 624-630.
42. Schafers, M., Brinkhoff, J., Neukirchen, S., Marziniak, M. & Sommer, C. (2001) Combined epineurial therapy with neutralizing antibodies to tumor necrosis factor-alpha and interleukin-1 receptor has an additive effect in reducing neuropathic pain in mice. Neurosci. Lett., 310, 113-116.
43. Sommer, C., Schafers, M., Marziniak, M. & Toyka, K.V. (2001) Etanercept reduces hyperalgesia in experimental painful neuropathy. J. Peripheral Nerv. Sys., 6, 67-72.
44. Sweitzer, S., Martin, D. & Deteo, J.A. (2001) Intrathecal interleukin-1 receptor antagonist in combination with soluble tumor necrosis factor receptor exhibits an anti-allodynic action in a rat model of neuropathic pain. Neuroscience. 103, 529-539.
45. Szklarczyk, A., Lapinska, J., Rylaski, M., McKay, R.D. & Kaczmarek, L. (2002) Matrix metalloproteinase-9 undergoes expression and activation during dendritic remodeling in adult hippocampus. J. Neurosci. 22. 920-930.
46. Tikka, T.M. & Koistinaho, J.E. (2001) Minocycline provides neuroprotection against N-methyl-D-aspartate neurotoxicity by inhibiting microglia. J. Immunol., 166, 7527-7533.
47. Treutwein, B. & Strasburger, H. (1999) Fitting the psychometric function. Percept Psychophys., 61, 87-106.
48. Twining, C.M., Sloane, E.M., Milligan, E.D., Chacur, M., Martin, D., Poole, S., Marsh, K. Maier, S.F. & Watkins, L.R. (2004) Peri-sciatic proinflammatory cytokines, reactive oxygen species, and complement induce mirror-image neuropathic pain in rats. Pain, 110, 299-309.
49. Verge, G.M., Milligan, E.D., Maier, S.F., Watkins, L.R., Naeve, G.S. & Foster, A.C. (2004) Fractalkine (CX3CL1) and fractalkine receptor (CX3CR1) distribution in spinal cord and dorsal root ganglia (DRG) under basal versus neuropathic pain conditions. Eur. J. Neurosci., 20, 1150-1160.
50. Watkins, L.R. & Maier, S.F. (2002) Beyond neurons: evidence that immune and glial cells contribute to pathological pain states. Physiol. Rev., 82, 981-1011.
51. Watkins, L.R. & Maier, S.F. (2003) Glia: a novel drug discovery target for clinical pain. Nature Rev. Drug Discovery. 2, 973-985.
52. Watkins, L.R., Milligan, E.D. & Maier, S.F. (2001) Glial activation: a driving force for pathological pain. Trends Neurosci., 24, 450-455.
53. Wienrich, M. & Kettenmann, H. (1989) Activation of substance P receptors leads to membrane potential responses in cultured astrocytes. Glia, 2, 155-160.