Influence of the vanilloid receptor TRPV1 on the activation of spinal cord glia in mouse models of pain

Experimental Neurology

Volumn 220, Issue 2, 2009, Pages 383-390

  Chen, Yong ^a   Willcockson, Helen H ^a   Valtschanoff, Juli G ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Astrocytes; Glia; Microglia; Mouse; Spinal cord; TRPV 1

Indexed keywords

BINDING PROTEIN; CAPSAICIN; GLIAL FIBRILLARY ACIDIC PROTEIN; IONIZED CALCIUM BINDING ADAPTER MOLECULE 1; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTHRALGIA; ARTHRITIS; ARTICLE; ASTROCYTE; CONTROLLED STUDY; GLIA; MALE; MICROGLIA; MOUSE; NERVE LIGATION; NEUROPATHIC PAIN; NONHUMAN; PAIN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SPINAL CORD;

ANIMALS; ARTHRITIS, EXPERIMENTAL; BEHAVIOR, ANIMAL; BIOLOGICAL MARKERS; GLIAL FIBRILLARY ACIDIC PROTEIN; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUROGLIA; PAIN; PERIPHERAL NERVES; PERIPHERAL NERVOUS SYSTEM DISEASES; SPINAL CORD; TRPV CATION CHANNELS;

EID: 71549147547     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2009.09.030     Document Type: Article

References (55)

1. Amantini C., Mosca M., Nabissi M., Lucciarini R., Caprodossi S., Arcella A., Giangaspero F., and Santoni G. Capsaicin-induced apoptosis of glioma cells is mediated by TRPV1 vanilloid receptor and requires p38 MAPK activation. J. Neurochem. 102 (2007) 977-990
2. Basu S., and Srivastava P. Immunological role of neuronal receptor vanilloid receptor 1 expressed on dendritic cells. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 5120-5125
3. Binshtok A.M., Wang H., Zimmermann K., Amaya F., Vardeh D., Shi L., Brenner G.J., Ji R.R., Bean B.P., Woolf C.J., and Samad T.A. Nociceptors are interleukin-1beta sensors. J. Neurosci. 28 (2008) 14062-14073
4. Bolcskei K., Helyes Z., Szabo A., Sandor K., Elekes K., Nemeth J., Almasi R., Pinter E., Petho G., and Szolcsanyi J. Investigation of the role of TRPV1 receptors in acute and chronic nociceptive processes using gene-deficient mice. Pain 117 (2005) 368-376
5. Cannon G.W., Woods M.L., Clayton F., and Griffiths M.M. Induction of arthritis in DA rats by incomplete Freund's adjuvant. J. Rheumatol. 20 (1993) 7-11
6. Caterina M.J., Schumacher M.A., Tominaga M., Rosen T.A., Levine J.D., and Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389 (1997) 816-824
7. Cho W.G., and Valtschanoff J.G. Vanilloid receptor TRPV1-positive sensory afferents in the mouse ankle and knee joints. Brain Res. 1219 (2008) 59-65
8. Christoph T., Grunweller A., Mika J., Schafer M.K., Wade E.J., Weihe E., Erdmann V.A., Frank R., Gillen C., and Kurreck J. Silencing of vanilloid receptor TRPV1 by RNAi reduces neuropathic and visceral pain in vivo. Biochem. Biophys. Res. Commun. 350 (2006) 238-243
9. Christoph T., Gillen C., Mika J., Grunweller A., Schafer M.K., Schiene K., Frank R., Jostock R., Bahrenberg G., Weihe E., Erdmann V.A., and Kurreck J. Antinociceptive effect of antisense oligonucleotides against the vanilloid receptor VR1/TRPV1. Neurochem. Int. 50 (2007) 281-290
10. Cui M., Honore P., Zhong C., Gauvin D., Mikusa J., Hernandez G., Chandran P., Gomtsyan A., Brown B., Bayburt E.K., Marsh K., Bianchi B., McDonald H., Niforatos W., Neelands T.R., Moreland R.B., Decker M.W., Lee C.H., Sullivan J.P., and Faltynek C.R. TRPV1 receptors in the CNS play a key role in broad-spectrum analgesia of TRPV1 antagonists. J. Neurosci. 26 (2006) 9385-9393
11. D'Mello R., and Dickenson A.H. Spinal cord mechanisms of pain. Br. J. Anaesth. 101 (2008) 8-16
12. Dansereau M.A., Gosselin R.D., Pohl M., Pommier B., Mechighel P., Mauborgne A., Rostene W., Kitabgi P., Beaudet N., Sarret P., and Melik-Parsadaniantz S. Spinal CCL2 pronociceptive action is no longer effective in CCR2 receptor antagonist-treated rats. J. Neurochem. 106 (2008) 757-769
13. Doly S., Fischer J., Salio C., and Conrath M. The vanilloid receptor-1 is expressed in rat spinal dorsal horn astrocytes. Neurosci. Lett. 357 (2004) 123-126
14. Eng L.F., Ghirnikar R.S., and Lee Y.L. Glial fibrillary acidic protein: GFAP-thirty-one years (1969-2000). Neurochem. Res. 25 (2000) 1439-1451
15. Fiacco T.A., Agulhon C., and McCarthy K.D. Sorting out astrocyte physiology from pharmacology. Annu. Rev. Pharmacol. Toxicol. 49 (2009) 151-174
16. Fiorentino P.M., Tallents R.H., Miller J.N., Brouxhon S.M., O'Banion M.K., Puzas J.E., and Kyrkanides S. Spinal interleukin-1beta in a mouse model of arthritis and joint pain. Arthritis. Rheum. 58 (2008) 3100-3109
17. Fu K.Y., Light A.R., and Maixner W. Relationship between nociceptor activity, peripheral edema, spinal microglial activation and long-term hyperalgesia induced by formalin. Neuroscience 101 (2000) 1127-1135
18. Hargreaves K., Dubner R., Brown F., Flores C., and Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32 (1988) 77-88
19. Hathway G.J., Vega-Avelaira D., Moss A., Ingram R., and Fitzgerald M. Brief, low frequency stimulation of rat peripheral C-fibres evokes prolonged microglial-induced central sensitization in adults but not in neonates. Pain 144 (2009) 110-118
20. Hensellek S., Brell P., Schaible H.G., Brauer R., and Segond von Banchet G. The cytokine TNFalpha increases the proportion of DRG neurones expressing the TRPV1 receptor via the TNFR1 receptor and ERK activation. Mol. Cell. Neurosci. 36 (2007) 381-391
21. Honore P., Wismer C.T., Mikusa J., Zhu C.Z., Zhong C., Gauvin D.M., Gomtsyan A., El Kouhen R., Lee C.H., Marsh K., Sullivan J.P., Faltynek C.R., and Jarvis M.F. A-425619 [1-isoquinolin-5-yl-3-(4-trifluoromethyl-benzyl)-urea], a novel transient receptor potential type V1 receptor antagonist, relieves pathophysiological pain associated with inflammation and tissue injury in rats. J. Pharmacol. Exp. Ther. 314 (2005) 410-421
22. Hwang S.J., Burette A., Rustioni A., and Valtschanoff J.G. Vanilloid receptor VR1-positive primary afferents are glutamatergic and contact spinal neurons that co-express neurokinin receptor NK1 and glutamate receptors. J. Neurocytol. 33 (2004) 321-329
23. Imai Y., and Kohsaka S. Intracellular signaling in M-CSF-induced microglia activation: role of Iba1. Glia 40 (2002) 164-174
24. Imai Y., Ibata I., Ito D., Ohsawa K., and Kohsaka S. A novel gene iba1 in the major histocompatibility complex class III region encoding an EF hand protein expressed in a monocytic lineage. Biochem. Biophys. Res. Commun. 224 (1996) 855-862
25. Ito D., Tanaka K., Suzuki S., Dembo T., and Fukuuchi Y. Enhanced expression of Iba1, ionized calcium-binding adapter molecule 1, after transient focal cerebral ischemia in rat brain. Stroke 32 (2001) 1208-1215
26. Ji R.R., and Suter M.R. p38 MAPK, microglial signaling, and neuropathic pain. Mol. Pain 3 (2007) 33
27. Jin Y.H., Yamaki F., Takemura M., Koike Y., Furuyama A., and Yonehara N. Capsaicin-induced glutamate release is implicated in nociceptive processing through activation of ionotropic glutamate receptors and group I metabotropic glutamate receptor in primary afferent fibers. J. Pharmacol. Sci. 109 (2009) 233-241
28. Jung H., Toth P.T., White F.A., and Miller R.J. Monocyte chemoattractant protein-1 functions as a neuromodulator in dorsal root ganglia neurons. J. Neurochem. 104 (2008) 254-263
29. Kanai Y., Nakazato E., Fujiuchi A., Hara T., and Imai A. Involvement of an increased spinal TRPV1 sensitization through its up-regulation in mechanical allodynia of CCI rats. Neuropharmacology 49 (2005) 977-984
30. Katanosaka K., Banik R.K., Giron R., Higashi T., Tominaga M., and Mizumura K. Contribution of TRPV1 to the bradykinin-evoked nociceptive behavior and excitation of cutaneous sensory neurons. Neurosci. Res. 62 (2008) 168-175
31. Kim S.R., Kim S.U., Oh U., and Jin B.K. Transient receptor potential vanilloid subtype 1 mediates microglial cell death in vivo and in vitro via Ca2+-mediated mitochondrial damage and cytochrome c release. J. Immunol. 177 (2006) 4322-4329
32. Kissin I. Vanilloid-induced conduction analgesia: selective, dose-dependent, long-lasting, with a low level of potential neurotoxicity. Anesth. Analg. 107 (2008) 271-281
33. Koltzenburg M., Wall P.D., and McMahon S.B. Does the right side know what the left is doing?. Trends Neurosci. 22 (1999) 122-127
34. Lappin S.C., Randall A.D., Gunthorpe M.J., and Morisset V. TRPV1 antagonist, SB-366791, inhibits glutamatergic synaptic transmission in rat spinal dorsal horn following peripheral inflammation. Eur. J. Pharmacol. 540 (2006) 73-81
35. Levine J.D., and Alessandri-Haber N. TRP channels: targets for the relief of pain. Biochim. Biophys. Acta 1772 (2007) 989-1003
36. Lin T., Li K., Zhang F.Y., Zhang Z.K., Light A.R., and Fu K.Y. Dissociation of spinal microglia morphological activation and peripheral inflammation in inflammatory pain models. J. Neuroimmunol. 192 (2007) 40-48
37. Milligan E.D., and Watkins L.R. Pathological and protective roles of glia in chronic pain. Nat. Rev. Neurosci. 10 (2009) 23-36
38. Obata H., Eisenach J.C., Hussain H., Bynum T., and Vincler M. Spinal glial activation contributes to postoperative mechanical hypersensitivity in the rat. J. Pain 7 (2006) 816-822
39. Pekny M., and Pekna M. Astrocyte intermediate filaments in CNS pathologies and regeneration. J. Pathol. 204 (2004) 428-437
40. Romero-Sandoval A., Chai N., Nutile-McMenemy N., and Deleo J.A. A comparison of spinal Iba1 and GFAP expression in rodent models of acute and chronic pain. Brain Res. 1219 (2008) 116-126
41. Sandkuhler J. Models and mechanisms of hyperalgesia and allodynia. Physiol. Rev. 89 (2009) 707-758
42. Sappington R.M., and Calkins D.J. Contribution of TRPV1 to microglia-derived IL-6 and NFkappaB translocation with elevated hydrostatic pressure. Invest. Ophthalmol. Vis. Sci. 49 (2008) 3004-3017
43. Schnizler K., Shutov L.P., Van Kanegan M.J., Merrill M.A., Nichols B., McKnight G.S., Strack S., Hell J.W., and Usachev Y.M. Protein kinase A anchoring via AKAP150 is essential for TRPV1 modulation by forskolin and prostaglandin E2 in mouse sensory neurons. J. Neurosci. 28 (2008) 4904-4917
44. Scholz J., and Woolf C.J. The neuropathic pain triad: neurons, immune cells and glia. Nat. Neurosci. 10 (2007) 1361-1368
45. Seltzer Z., Dubner R., and Shir Y. A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury. Pain 43 (1990) 205-218
46. Shapiro L.A., Perez Z.D., Foresti M.L., Arisi G.M., and Ribak C.E. Morphological and ultrastructural features of Iba1-immunolabeled microglial cells in the hippocampal dentate gyrus. Brain Res. 1266 (2009) 29-36
47. Sun S., Cao H., Han M., Li T.T., Pan H.L., Zhao Z.Q., and Zhang Y.Q. New evidence for the involvement of spinal fractalkine receptor in pain facilitation and spinal glial activation in rat model of monoarthritis. Pain 129 (2007) 64-75
48. Szabo A., Helyes Z., Sandor K., Bite A., Pinter E., Nemeth J., Banvolgyi A., Bolcskei K., Elekes K., and Szolcsanyi J. Role of transient receptor potential vanilloid 1 receptors in adjuvant-induced chronic arthritis: in vivo study using gene-deficient mice. J. Pharmacol. Exp. Ther. 314 (2005) 111-119
49. Szallasi A., Cortright D.N., Blum C.A., and Eid S.R. The vanilloid receptor TRPV1: 10 years from channel cloning to antagonist proof-of-concept. Nat. Rev. Drug. Discov. 6 (2007) 357-372
50. Tanga F.Y., Raghavendra V., and DeLeo J.A. Quantitative real-time RT-PCR assessment of spinal microglial and astrocytic activation markers in a rat model of neuropathic pain. Neurochem. Int. 45 (2004) 397-407
51. Tominaga M., Caterina M.J., Malmberg A.B., Rosen T.A., Gilbert H., Skinner K., Raumann B.E., Basbaum A.I., and Julius D. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21 (1998) 531-543
52. Tsuda M., Inoue K., and Salter M.W. Neuropathic pain and spinal microglia: a big problem from molecules in "small" glia. Trends Neurosci. 28 (2005) 101-107
53. Wilson-Gerwing T.D., Dmyterko M.V., Zochodne D.W., Johnston J.M., and Verge V.M. Neurotrophin-3 suppresses thermal hyperalgesia associated with neuropathic pain and attenuates transient receptor potential vanilloid receptor-1 expression in adult sensory neurons. J. Neurosci. 25 (2005) 758-767
54. Zhou H.Y., Chen S.R., Chen H., and Pan H.L. The glutamatergic nature of TRPV1-expressing neurons in the spinal dorsal horn. J. Neurochem. 108 (2009) 305-318
55. Zhuang Z.Y., Gerner P., Woolf C.J., and Ji R.R. ERK is sequentially activated in neurons, microglia, and astrocytes by spinal nerve ligation and contributes to mechanical allodynia in this neuropathic pain model. Pain 114 (2005) 149-159