CCL2 has similar excitatory effects to TNF-α in a subgroup of inflamed C-fiber axons

Journal of Neurophysiology

Volumn 106, Issue 6, 2011, Pages 2838-2848

  Richards, Natalie ^a   Batty, Thomas ^a   Dilley, Andrew ^a  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

Author keywords

Chronic pain; Cytokines; Electrophysiology; Nociceptors; Ongoing activity

Indexed keywords

CHEMOKINE RECEPTOR; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR;

ANESTHESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; CONTROLLED STUDY; ELECTROPHYSIOLOGY; GLIA; IMMUNOHISTOCHEMISTRY; NERVE CELL LESION; NERVE CELL STIMULATION; NERVE CONDUCTION; NERVE FIBER C; NEURITIS; NONHUMAN; PRIORITY JOURNAL; RAT; STIMULUS RESPONSE;

ACTION POTENTIALS; ANIMALS; AXONS; CHEMOKINE CCL2; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; GANGLIA, SPINAL; GENE EXPRESSION REGULATION; MALE; NERVE FIBERS, UNMYELINATED; NEURAL CONDUCTION; NEURITIS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CYTOKINE; SCIATIC NERVE; SPINAL NERVES; STATISTICS, NONPARAMETRIC; TUMOR NECROSIS FACTOR-ALPHA;

EID: 83055165974     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00183.2011     Document Type: Article

References (57)

1. Abbadie C, Lindia JA, Cumiskey AM, Peterson LB, Mudgett JS, Bayne EK, DeMartino JA, MacIntyre DE, Forrest MJ. Impaired neuropathic pain responses in mice lacking the chemokine receptor CCR2. Proc Natl Acad Sci USA 100: 7947-7952, 2003.
2. Bessou P, Perl ER. Response of cutaneous sensory units with unmyelinated fibers to noxious stimuli. J Neurophysiol 32: 1025-1043, 1969.
3. Bhangoo S, Ren D, Miller RJ, Henry KJ, Lineswala J, Hamdouchi C, Li B, Monahan PE, Chan DM, Ripsch MS, White FA. Delayed functional expression of neuronal chemokine receptors following focal nerve demyelination in the rat: a mechanism for the development of chronic sensitization of peripheral nociceptors. Mol Pain 3: 38, 2007.
4. Black JA, Liu S, Tanaka M, Cummins TR, Waxman SG. Changes in the expression of tetrodotoxin-sensitive sodium channels within dorsal root ganglia neurons in inflammatory pain. Pain 108: 237-247, 2004.
5. Bove GM. Focal nerve inflammation induces neuronal signs consistent with symptoms of early complex regional pain syndromes. Exp Neurol 219: 223-227, 2009.
6. Bove GM, Dilley A. The conundrum of sensitization when recording from nociceptors. J Neurosci Methods 188: 213-218, 2010.
7. Bove GM, Ransil BJ, Lin HC, Leem JG. Inflammation induces ectopic mechanical sensitivity in axons of nociceptors innervating deep tissues. J Neurophysiol 90: 1949-1955, 2003.
8. Chacur M, Milligan ED, Gazda LS, Armstrong C, Wang HC, Tracey KJ, Maier SF, Watkins LR. 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, 2001.
9. Chen Y, Devor M. Ectopic mechanosensitivity in injured sensory axons arises from the site of spontaneous electrogenesis. Eur J Pain 2: 165-178, 1998.
10. Coderre TJ, Bennett GJ. A hypothesis for the cause of complex regional pain syndrome-type I (reflex sympathetic dystrophy): pain due to deep-tissue microvascular pathology. Pain Med 11: 1224-1238, 2010.
11. Czeschik JC, Hagenacker T, Schafers M, Busselberg D. TNF-alpha differentially modulates ion channels of nociceptive neurons. Neurosci Lett 434: 293-298, 2008.
12. de Mos M, Sturkenboom MC, Huygen FJ. Current understandings on complex regional pain syndrome. Pain Pract 9: 86-99, 2009.
13. Dilley A, Bove GM. Disruption of axoplasmic transport induces mechanical sensitivity in intact rat C-fibre nociceptor axons. J Physiol 586: 593-604, 2008a.
14. Dilley A, Bove GM. Resolution of inflammation-induced axonal mechanical sensitivity and conduction slowing in C-fiber nociceptors. J Pain 9: 185-192, 2008b.
15. Dilley A, Greening J, Walker-Bone K, Good C. MRI signal hyper-intensity of neural tissues in diffuse chronic pain syndromes-a pilot study. Muscle Nerve. In press.
16. Dilley A, Lynn B, Pang SJ. Pressure and stretch mechanosensitivity of peripheral nerve fibres following local inflammation of the nerve trunk. Pain 117: 462-472, 2005.
17. Eliav E, Benoliel R, Herzberg U, Kalladka M, Tal M. The role of IL-6 and IL-1beta in painful perineural inflammatory neuritis. Brain Behav Immun 23: 474-484, 2009.
18. Eliav E, Benoliel R, Tal M. Inflammation with no axonal damage of the rat saphenous nerve trunk induces ectopic discharge and mechanosensitivity in myelinated axons. Neurosci Lett 311: 49-52, 2001.
19. Eliav E, Herzberg U, Ruda MA, Bennett GJ. Neuropathic pain from an experimental neuritis of the rat sciatic nerve. Pain 83: 169-182, 1999.
20. Elliott MB, Barr AE, Kietrys DM, Al-Shatti T, Amin M, Barbe MF. Peripheral neuritis and increased spinal cord neurochemicals are induced in a model of repetitive motion injury with low force and repetition exposure. Brain Res 1218: 103-113, 2008.
21. Gazda LS, Milligan ED, Hansen MK, Twining CM, Poulos NM, Chacur M, O'Connor KA, Armstrong C, Maier SF, Watkins LR, Myers RR. Sciatic inflammatory neuritis (SIN): behavioral allodynia is paralleled by peri-sciatic proinflammatory cytokine and superoxide production. J Peripher Nerv Syst 6: 111-129, 2001.
22. George A, Buehl A, Sommer C. Tumor necrosis factor receptor 1 and 2 proteins are differentially regulated during Wallerian degeneration of mouse sciatic nerve. Exp Neurol 192: 163-166, 2005.
23. Gold MS, Weinreich D, Kim CS, Wang R, Treanor J, Porreca F, Lai J. Redistribution of Na(V)1.8 in uninjured axons enables neuropathic pain. J Neurosci 23: 158-166, 2003.
24. Gracely RH, Lynch SA, Bennett GJ. Painful neuropathy: altered central processing maintained dynamically by peripheral input. Pain 51: 175-194, 1992.
25. Grossmann L, Gorodetskaya N, Baron R, Janig W. Enhancement of ectopic discharge in regenerating A- and C-fibers by inflammatory mediators. J Neurophysiol 101: 2762-2774, 2009.
26. Howe JF, Loeser JD, Calvin WH. Mechanosensitivity of dorsal root ganglia and chronically injured axons: a physiological basis for the radicular pain of nerve root compression. Pain 3: 25-41, 1977.
27. Janig W, Baron R. Complex regional pain syndrome: mystery explained? Lancet Neurol 2: 687-697, 2003.
28. Jiang YQ, Xing GG, Wang SL, Tu HY, Chi YN, Li J, Liu FY, Han JS, Wan Y. Axonal accumulation of hyperpolarization-activated cyclic nucleotide- gated cation channels contributes to mechanical allodynia after peripheral nerve injury in rat. Pain 137: 495-506, 2008.
29. Jin X, Gereau RW 4th. Acute p38-mediated modulation of tetrodotoxinresistant sodium channels in mouse sensory neurons by tumor necrosis factor-alpha. J Neurosci 26: 246-255, 2006.
30. Jung H, Bhangoo S, Banisadr G, Freitag C, Ren D, White FA, Miller RJ. Visualization of chemokine receptor activation in transgenic mice reveals peripheral activation of CCR2 receptors in states of neuropathic pain. J Neurosci 29: 8051-8062, 2009.
31. Jung H, Toth PT, White FA, Miller RJ. Monocyte chemoattractant protein-1 functions as a neuromodulator in dorsal root ganglia neurons. J Neurochem 104: 254-263, 2008.
32. Leem JG, Bove GM. Mid-axonal tumor necrosis factor-alpha induces ectopic activity in a subset of slowly conducting cutaneous and deep afferent neurons. J Pain 3: 45-49, 2002.
33. Liu B, Li HQ, Brull SJ, Zhang JM. Increased sensitivity of sensory neurons to tumor necrosis factor αB1; in rats with chronic compression of the lumbar ganglia. J Neurophysiol 88: 1393-1399, 2002.
34. Liu BG, Dobretsov M, Stimers JR, Zhang JM. Tumor necrosis factor-alpha suppresses activation of sustained potassium currents in rat small diameter sensory neurons. Open Pain J 1: 1, 2008.
35. Michaelis M, Blenk KH, Janig W, Vogel C. Development of spontaneous activity and mechanosensitivity in axotomized afferent nerve fibers during the first hours after nerve transection in rats. J Neurophysiol 74: 1020-1027, 1995.
36. Oh SB, Tran PB, Gillard SE, Hurley RW, Hammond DL, Miller RJ. Chemokines and glycoprotein120 produce pain hypersensitivity by directly exciting primary nociceptive neurons. J Neurosci 21: 5027-5035, 2001.
37. 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 20: 6289-6293, 2000.
38. Perl ER, Kumazawa T, Lynn B, Kenins P. Sensitization of high threshold receptors with unmyelinated (C) afferent fibers. Prog Brain Res 43: 263-277, 1976.
39. Qin X, Wan Y, Wang X. CCL2 and CXCL1 trigger calcitonin gene-related peptide release by exciting primary nociceptive neurons. J Neurosci Res 82: 51-62, 2005.
40. Scadding JW. Development of ongoing activity, mechanosensitivity, and adrenaline sensitivity in severed peripheral nerve axons. Exp Neurol 73: 345-364, 1981.
41. Schafers M, Lee DH, Brors D, Yaksh TL, Sorkin LS. Increased sensitivity of injured and adjacent uninjured rat primary sensory neurons to exogenous tumor necrosis factor-alpha after spinal nerve ligation. J Neurosci 23: 3028-3038, 2003.
42. Schafers M, Sommer C, Geis C, Hagenacker T, Vandenabeele P, Sorkin LS. Selective stimulation of either tumor necrosis factor receptor differentially induces pain behavior in vivo and ectopic activity in sensory neurons in vitro. Neuroscience 157: 414-423, 2008.
43. Shubayev VI, Myers RR. Upregulation and interaction of TNF alpha and gelatinases A and B in painful peripheral nerve injury. Brain Res 855: 83-89, 2000.
44. Sorkin LS, Xiao WH, Wagner R, Myers RR. Tumour necrosis factor-alpha induces ectopic activity in nociceptive primary afferent fibres. Neuroscience 81: 255-262, 1997.
45. Sun JH, Yang B, Donnelly DF, Ma C, LaMotte RH. MCP-1 enhances excitability of nociceptive neurons in chronically compressed dorsal root ganglia. J Neurophysiol 96: 2189-2199, 2006.
46. Tal M, Eliav E. Abnormal discharge originates at the site of nerve injury in experimental constriction neuropathy (CCI) in the rat. Pain 64: 511-518, 1996.
47. Tanaka T, Minami M, Nakagawa T, Satoh M. Enhanced production of monocyte chemoattractant protein-1 in the dorsal root ganglia in a rat model of neuropathic pain: possible involvement in the development of neuropathic pain. Neurosci Res 48: 463-469, 2004.
48. Thacker MA, Clark AK, Bishop T, Grist J, Yip PK, Moon LD, Thompson SW, Marchand F, McMahon SB. CCL2 is a key mediator of microglia activation in neuropathic pain states. Eur J Pain 13: 263-272, 2009.
49. Upton ARM, McComas AJ. The double crush in nerve entrapment syndromes. Lancet 2: 359-362, 1973.
50. Wagner R, Myers RR. Endoneurial injection of TNF-alpha produces neuropathic pain behaviors. Neuroreport 7: 2897-2901, 1996.
51. Wang CH, Zou LJ, Zhang YL, Jiao YF, Sun JH. The excitatory effects of the chemokine CCL2 on DRG somata are greater after an injury of the ganglion than after an injury of the spinal or peripheral nerve. Neurosci Lett 475: 48-52, 2010.
52. White FA, Sun J, Waters SM, Ma C, Ren D, Ripsch M, Steflik J, Cortright DN, Lamotte RH, Miller RJ. Excitatory monocyte chemoattractant protein- 1 signaling is up-regulated in sensory neurons after chronic compression of the dorsal root ganglion. Proc Natl Acad Sci USA 102: 14092-14097, 2005.
53. Xia RH, Yosef N, Ubogu EE. Selective expression and cellular localization of pro-inflammatory chemokine ligand/receptor pairs in the sciatic nerves of a severe murine experimental autoimmune neuritis model of Guillain-Barre syndrome. Neuropathol Appl Neurobiol 36: 388-398, 2010.
54. Yang HY, Mitchell K, Keller JM, Iadarola MJ. Peripheral inflammation increases Scya2 expression in sensory ganglia and cytokine and endothelial related gene expression in inflamed tissue. J Neurochem 103: 1628-1643, 2007.
55. You H, Altier C, Zamponi GW. CCR2 receptor ligands inhibit Cav3.2 T-type calcium channels. Mol Pharmacol 77: 211-217, 2010.
56. Zelenka M, Schafers M, Sommer C. Intraneural injection of interleukin- 1beta and tumor necrosis factor-alpha into rat sciatic nerve at physiological doses induces signs of neuropathic pain. Pain 116: 257-263, 2005.
57. Zhang JM, Li HQ, Liu B, Brull SJ. Acute topical application of tumor necrosis factor α evokes protein kinase A-dependent responses in rat sensory neurons. J Neurophysiol 88: 1387-1392, 2002.