Implication of the chemokine CCL2 in trigeminal nociception and traumatic neuropathic orofacial pain

European Journal of Pain (United Kingdom)

Volumn 18, Issue 3, 2014, Pages 360-375

  Dauvergne, C ^a,b   Molet, J ^a   Reaux Le Goazigo, A ^c   Mauborgne, A ^a   Melik Parsadaniantz S ^c   Boucher, Y ^a,b   Pohl, M ^a  

^a INSTITUT DU CERVEAU ET DE LA MOELLE ÉPINIÈRE   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c INSTITUT DE LA VISION   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTEGRIN; CD11B ANTIGEN; INTERLEUKIN 1BETA; INTERLEUKIN 6; ISOLECTIN B4; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; N [2 [[1 [4 (1,3 BENZODIOXOL 5 YL) 4 HYDROXYCYCLOHEXYL] 4 ETHOXY 3 PYRROLIDINYL]AMINO] 2 OXOETHYL] 3 (TRIFLUOROMETHYL)BENZAMIDE; NEURON SPECIFIC NUCLEAR PROTEIN; CCR2 PROTEIN, RAT; CHEMOKINE RECEPTOR CCR2; PYRROLIDINE DERIVATIVE;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHRONIC CONSTRICTION INJURY; CONTROLLED STUDY; EVOKED SOMATOSENSORY RESPONSE; GANGLION; HYPERSENSITIVITY; IMMUNOHISTOCHEMISTRY; INFRAORBITAL NERVE; MALE; MECHANICAL STIMULATION; MICROGLIA; NERVE CELL PLASTICITY; NEUROPATHIC PAIN; NOCICEPTION; NONHUMAN; OROFACIAL PAIN; PAIN THRESHOLD; PRIORITY JOURNAL; RAT; SOMATOSENSORY SYSTEM; TRIGEMINAL NERVE; TRIGEMINAL NERVE INJURY; TRIGEMINAL NUCLEUS; TRIGEMINUS NEURALGIA; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; FACE PAIN; HYPERALGESIA; METABOLISM; NEURALGIA; PHYSIOLOGY; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; TRIGEMINUS GANGLION;

ANIMALS; CHEMOKINE CCL2; FACIAL PAIN; HYPERALGESIA; MALE; NEURALGIA; NOCICEPTION; PYRROLIDINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CCR2; SIGNAL TRANSDUCTION; TRIGEMINAL GANGLION;

EID: 84898910736     PISSN: 10903801     EISSN: 15322149     Source Type: Journal    
DOI: 10.1002/j.1532-2149.2013.00377.x     Document Type: Article

References (63)

1. Abbadie, C., Bhangoo, S., De Koninck, Y., Malcangio, M., Melik-Parsadaniantz, S., White, F.A., (2009). Chemokines and pain mechanisms. Brain Res Rev 60, 125-134.
2. 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 U S A 100, 7947-7952.
3. Ahn, D.K., Lee, K.R., Lee, H.J., Kim, S.K., Choi, H.S., Lim, E.J., Park, J.S., (2005). Intracisternal administration of chemokines facilitated formalin-induced behavioral responses in the orofacial area of freely moving rats. Brain Res Bull 66, 50-58.
4. Aita, M., Byers, M.R., Chavkin, C., Xu, M., (2010). Trigeminal injury causes kappa opioid-dependent allodynic, glial and immune cell responses in mice. Mol Pain 6, 8.
5. Attal, N., Filliatreau, G., Perrot, S., Jazat, F., Di Giamberardino, L., Guilbaud, G., (1994). Behavioural pain-related disorders and contribution of the saphenous nerve in crush and chronic constriction injury of the rat sciatic nerve. Pain 59, 301-312.
6. Austin, P.J., Moalem-Taylor, G., (2010). The neuro-immune balance in neuropathic pain: Involvement of inflammatory immune cells, immune-like glial cells and cytokines. J Neuroimmunol 229, 26-50.
7. Bae, Y.C., Oh, J.M., Hwang, S.J., Shigenaga, Y., Valtschanoff, J.G., (2004). Expression of vanilloid receptor TRPV1 in the rat trigeminal sensory nuclei. J Comp Neurol 478, 62-71.
8. Banisadr, G., Gosselin, R.-D., Mechighel, P., Kitabgi, P., Rostène, W., Parsadaniantz, S.M., (2005). Highly regionalized neuronal expression of monocyte chemoattractant protein-1 (MCP-1/CCL2) in rat brain: Evidence for its colocalization with neurotransmitters and neuropeptides. J Comp Neurol 489, 275-292.
9. Banisadr, G., Quéraud-Lesaux, F., Boutterin, M.C., Pélaprat, D., Zalc, B., Rostène, W., Haour, F., Parsadaniantz, S.M., (2002). Distribution, cellular localization and functional role of CCR2 chemokine receptors in adult rat brain. J Neurochem 81, 257-269.
10. Belkouch, M., Dansereau, M.-A., Réaux-Le Goazigo, A., Van Steenwinckel, J., Beaudet, N., Chraibi, A., Melik-Parsadaniantz, S., Sarret, P., (2011). The chemokine CCL2 increases Nav1.8 sodium channel activity in primary sensory neurons through a Gβγ-dependent mechanism. J Neurosci 31, 18381-18390.
11. Bennett, G.J., Xie, Y.K., (1988). A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33, 87-107.
12. Benoliel, R., Eliav, E., Tal, M., (2001). No sympathetic nerve sprouting in rat trigeminal ganglion following painful and non-painful infraorbital nerve neuropathy. Neurosci Lett 297, 151-154.
13. Bongenhielm, U., Boissonade, F.M., Westermark, A., Robinson, P.P., Fried, K., (1999). Sympathetic nerve sprouting fails to occur in the trigeminal ganglion after peripheral nerve injury in the rat. Pain 82, 283-288.
14. Brodmerkel, C.M., Huber, R., Covington, M., Diamond, S., Hall, L., Collins, R., Leffet, L., Gallagher, K., Feldman, P., Collier, P., Stow, M., Gu, X., Baribaud, F., Shin, N., Thomas, B., Burn, T., Hollis, G., Yeleswaram, S., Solomon, K., Friedman, S., Wang, A., Xue, C.B., Newton, R.C., Scherle, P., Vaddi, K., (2005). Discovery and pharmacological characterization of a novel rodent-active CCR2 antagonist, INCB3344. J Immunol 175, 5370-5378.
15. Chiang, C.-Y., Dostrovsky, J.O., Iwata, K., Sessle, B.J., (2011). Role of glia in orofacial pain. Neuroscientist 17, 303-320.
16. Costigan, M., Moss, A., Latremoliere, A., Johnston, C., Verma-Gandhu, M., Herbert, T.A., Barret, L., Brenner, G.J., Vardeh, D., Woolf, C.J., Fitzgerald, M., (2009a). T-cell infiltration and signaling in the adult dorsal spinal cord is a major contributor to neuropathic pain-like hypersensitivity. J Neurosci 29, 14415-14422.
17. Costigan, M., Scholz, J., Woolf, C.J., (2009b). Neuropathic pain: A maladaptive response of the nervous system to damage. Annu Rev Neurosci 32, 1-32.
18. Coyle, D.E., (1998). Partial peripheral nerve injury leads to activation of astroglia and microglia which parallels the development of allodynic behavior. Glia 23, 75-83.
19. Cruccu, G., Leandri, M., Feliciani, M., Manfredi, M., (1990). Idiopathic and symptomatic trigeminal pain. J Neurol Neurosurg Psychiatry 53, 1034-1042.
20. Dallel, R., Raboisson, P., Auroy, P., Woda, A., (1988). The rostral part of the trigeminal sensory complex is involved in orofacial nociception. Brain Res 448, 7-19.
21. Dansereau, M.-A., Gosselin, R.-D., Pohl, M., Pommier, B., Mechighel, P., Mauborgne, A., Rostene, W., Kitabgi, P., Beaudet, N., Sarret, P., Melik-Parsadaniantz, S., (2008). Spinal CCL2 pronociceptive action is no longer effective in CCR2 receptor antagonist-treated rats. J Neurochem 106, 757-769.
22. Dominguez, E., Mauborgne, A., Mallet, J., Desclaux, M., Pohl, M., (2010). SOCS3-mediated blockade of JAK/STAT3 signaling pathway reveals its major contribution to spinal cord neuroinflammation and mechanical allodynia after peripheral nerve injury. J Neurosci 30, 5754-5766.
23. Gosselin, R.D., Varela, C., Banisadr, G., Mechighel, P., Rostene, W., Kitabgi, P., Melik-Parsadaniantz, S., (2005). Constitutive expression of CCR2 chemokine receptor and inhibition by MCP-1/CCL2 of GABA-induced currents in spinal cord neurones. J Neurochem 95, 1023-1034.
24. Guo, W., Wang, H., Watanabe, M., Shimizu, K., Zou, S., LaGraize, S.C., Wei, F., Dubner, R., Ren, K., (2007). Glial-cytokine-neuronal interactions underlying the mechanisms of persistent pain. J Neurosci 27, 6006-6018.
25. Hayashi, H., Sumino, R., Sessle, B.J., (1984). Functional organization of trigeminal subnucleus interpolaris: Nociceptive and innocuous afferent inputs, projections to thalamus, cerebellum, and spinal cord, and descending modulation from periaqueductal gray. J Neurophysiol 51, 890-905.
26. Howard, R.F., Walker, S.M., Mota, P.M., Fitzgerald, M., (2005). The ontogeny of neuropathic pain: postnatal onset of mechanical allodynia in rat spared nerve injury (SNI) and chronic constriction injury (CCI) models. Pain 115, 382-389.
27. Idänpään-Heikkilä, J.J., Guilbaud, G., (1999). Pharmacological studies on a rat model of trigeminal neuropathic pain: Baclofen, but not carbamazepine, morphine or tricyclic antidepressants, attenuates the allodynia-like behaviour. Pain 79, 281-290.
28. Jeon, S.-M., Lee, K.-M., Cho, H.-J., (2009). Expression of monocyte chemoattractant protein-1 in rat dorsal root ganglia and spinal cord in experimental models of neuropathic pain. Brain Res 1251, 103-111.
29. Katagiri, A., Shinoda, M., Honda, K., Toyofuku, A., Sessle, B.J., Iwata, K., (2012). Satellite glial cell P2Y12 receptor in the trigeminal ganglion is involved in lingual neuropathic pain mechanisms in rats. Mol Pain 30, 8-23.
30. Kayser, V., Viguier, F., Ioannidi, M., Bernard, J.-F., Latrémolière, A., Michot, B., Vela, J.-M., Buschmann, H., Hamon, M., Bourgoin, S., (2010). Differential anti-neuropathic pain effects of tetrodotoxin in sciatic nerve- versus infraorbital nerve-ligated rats-behavioral, pharmacological and immunohistochemical investigations. Neuropharmacology 58, 474-487.
31. Latrémolière, A., Mauborgne, A., Masson, J., Bourgoin, S., Kayser, V., Hamon, M., Pohl, M., (2008). Differential implication of proinflammatory cytokine interleukin-6 in the development of cephalic versus extracephalic neuropathic pain in rats. J Neurosci 28, 8489-8501.
32. Lee, S., Zhao, Y.Q., Ribeiro-Da-Silva, A., Zhang, J., (2010). Distinctive response of CNS glial cells in oro-facial pain associated with injury, infection and inflammation. Mol Pain 6, 79.
33. Livak, K.J., Schmittgen, T.D., (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)). Methods 25, 402-408.
34. Melzer, P., Zhang, M.Z., McKanna, J.A., (1997). Infraorbital nerve transection and whisker follicle removal in adult rats affect microglia and astrocytes in the trigeminal brainstem. A study with lipocortin1- and S100beta-immunohistochemistry. Neuroscience 80, 459-472.
35. Michot, B., Bourgoin, S., Viguier, F., Hamon, M., Kayser, V., (2012). Differential effects of calcitonin gene-related peptide receptor blockade by olcegepant on mechanical allodynia induced by ligation of the infraorbital nerve vs the sciatic nerve in the rat. Pain 153, 1939-1948.
36. Milligan, E.D., Watkins, L.R., (2009). Pathological and protective roles of glia in chronic pain. Nat Rev Neurosci 10, 23-36.
37. Narita, M., Yoshida, T., Nakajima, M., Narita, M., Miyatake, M., Takagi, T., Yajima, Y., Suzuki, T., (2006). Direct evidence for spinal cord microglia in the development of a neuropathic pain-like state in mice. J Neurochem 97, 1337-1348.
38. Okada-Ogawa, A., Suzuki, I., Sessle, B.J., Chiang, C.-Y., Salter, M.W., Dostrovsky, J.O., Tsuboi, Y., Kondo, M., Kitagawa, J., Kobayashi, A., Noma, N., Imamura, Y., Iwata, K., (2009). Astroglia in medullary dorsal horn (trigeminal spinal subnucleus caudalis) are involved in trigeminal neuropathic pain mechanisms. J Neurosci 29, 11161-11171.
39. Paxinos, G., Watson, C., (1997). The Rat Brain in Stereotaxic Coordinates (London: Academic Press).
40. Piao, Z.G., Cho, I.-H., Park, C.K., Hong, J.P., Choi, S.-Y., Lee, S.J., Lee, S., Park, K., Kim, J.S., Oh, S.B., (2006). Activation of glia and microglial p38 MAPK in medullary dorsal horn contributes to tactile hypersensitivity following trigeminal sensory nerve injury. Pain 121, 219-231.
41. Ren, K., Dubner, R., (2010). Interactions between the immune and nervous systems in pain. Nat Med 16, 1267-1276.
42. Scholz, J., Woolf, C.J., (2002). Can we conquer pain? Nat Neurosci 5 (Suppl), 1062-1067.
43. Scholz, J., Woolf, C.J., (2007). The neuropathic pain triad: Neurons, immune cells and glia. Nat Neurosci 10, 1361-1368.
44. Schwaiger, F.W., Hager, G., Schmitt, A.B., Horvat, A., Hager, G., Streif, R., Spitzer, C., Gamal, S., Breuer, S., Brook, G.A., Nacimiento, W., Kreutzberg, G.W., (2000). Peripheral but not central axotomy induces changes in Janus kinases (JAK) and signal transducers and activators of transcription (STAT). Eur J Neurosci 12, 1165-1176.
45. Sessle, B.J., (2000). Acute and chronic craniofacial pain: Brainstem mechanisms of nociceptive transmission and neuroplasticity, and their clinical correlates. Crit Rev Oral Biol Med 11, 57-91.
46. Shi, X.Q., Zekki, H., Zhang, J., (2011). The role of TLR2 signaling in nerve injury-induced neuropathic pain is essentially mediated through macrophages in peripheral inflammatory response. Glia 59, 234-241.
47. Shibuta, K., Suzuki, I., Shinoda, M., Tsuboi, Y., Honda, K., Shimizu, N., Sessle, B.J., Iwata, K., (2012). Organization of hyperactive microglial cells in trigeminal spinal subnucleuscaudalis and upper cervical spinal cord associated with orofacial neuropathic pain. Brain Res 27, 74-86.
48. Shimizu, K., Guo, W., Wang, H., Zou, S., LaGraize, S.C., Iwata, K., Wei, F., Dubner, R., Ren, K., (2009). Differential involvement of trigeminal transition zone and laminated subnucleus caudalis in orofacial deep and cutaneous hyperalgesia: The effects of interleukine-10 and glia inhibitors. Mol Pain 5, 75.
49. Takahashi, K., Watanabe, M., Suekawa, Y., Ito, G., Inubushi, T., Hirose, N., Murasaki, K., Hiyama, S., Uchida, T., Tanne, K., (2011). IL-beta in the trigeminal subnucleus caudalis contributes to extra-territorial allodynia/hyperalgesia following a trigeminal nerve injury. Eur J Pain 15, 467.e1-467.14.
50. Tal, M., Devor, M., (1992). Ectopic discharge in injured nerves: Comparison of trigeminal and somatic afferents. Brain Res 579, 148-151.
51. Tanaka, T., Minami, M., Nakagawa, T., Satoh, M., (2004). 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.
52. Thacker, M.A., Clark, A.K., Bishop, T., Grist, J., Yip, P.K., Moon, L.D.F., Thompson, S.W.N., Marchand, F., McMahon, S.B., (2009). CCL2 is a key mediator of microglia activation in neuropathic pain states. Eur J Pain 13, 263-272.
53. Van Steenwinckel, J., Reaux-Le Goazigo, A., Pommier, B., Mauborgne, A., Dansereau, M.-A., Kitabgi, P., Sarret, P., Pohl, M., Mélik-Parsadaniantz, S., (2011). CCL2 released from neuronal synaptic vesicles in the spinal cord is a major mediator of local inflammation and pain after peripheral nerve injury. J Neurosci 31, 5865-5875.
54. Vit, J., Jasmin, L., Bhargava, A., Ohara, P.T., (2006). Satellite glial cells in the trigeminal ganglion as a determinant of orofacial neuropathic pain. Neuron Glia Biol 2, 247-257.
55. Vos, B.P., Strassman, A.M., Maciewicz, R.J., (1994). Behavioral evidence of trigeminal neuropathic pain following chronic constriction injury to the rat's infraorbital nerve. J Neurosci 14, 2708-2723.
56. Wang, S., Lim, G., Mao, J., Sung, B., Mao, J., (2009). Regulation of the trigeminal NR1 subunit expression induced by inflammation of the temporomandibular joint region in rats. Pain 141, 97-103.
57. White, F.A., Jung, H., Miller, R.J., (2007). Chemokines and the pathophysiology of neuropathic pain. Proc Natl Acad Sci U S A 104, 20151-20158.
58. White, F.A., Sun, J., Waters, S.M., Ma, C., Ren, D., Ripsch, M., Steflik, J., Cortright, D.N., Lamotte, R.H., Miller, R.J., (2005). Excitatory monocyte chemoattractant protein-1 signaling is up-regulated in sensory neurons after chronic compression of the dorsal root ganglion. Proc Natl Acad Sci U S A 102, 14092-14097.
59. Winkelstein, B.A., Rutkowski, M.D., Sweitzer, S.M., Pahl, J.L., DeLeo, J.A., (2011). 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, 127-139.
60. Zhang, J., De Koninck, Y., (2006). Spatial and temporal relationship between monocyte chemoattractant protein-1 expression and spinal glial activation following peripheral nerve injury. J Neurochem 97, 772-783.
61. Zhang, J., Shi, X.Q., Echeverry, S., Mogil, J.S., De Koninck, Y., Rivest, S., (2007). Expression of CCR2 in both resident and bone marrow-derived microglia plays a critical role in neuropathic pain. J Neurosci 27, 12396-12406.
62. Zhang, Z.-J., Dong, Y.-L., Lu, Y., Cao, S., Zhao, Z.-Q., Gao, Y.-J., (2012). Chemokine CCL2 and its receptor CCR2 in the medullary dorsal horn are involved in trigeminal neuropathic pain. J Neuroinflammation 9, 136.
63. Zhou, Q., Imbe, H., Dubner, R., Ren, K., (1999). Persistent Fos protein expression after orofacial deep or cutaneous tissue inflammation in rats: Implications for persistent orofacial pain. J Comp Neurol 412, 276-291.