Browse > Article

Coexpression of $P2X_3$ with TRPV1 in the Rat Trigeminal Sensory Nuclei  

Moon, Yong-Suk (Department of Anatomy, School of Medicine, Catholic University of Daegu)
Ryoo, Chang-Hyun (Department of Oral Anatomy, School of Dentistry, Kyungpook National University)
Cho, Yi-Sul (Department of Oral Anatomy, School of Dentistry, Kyungpook National University)
Kim, Hong-Tae (Department of Anatomy, School of Medicine, Catholic University of Daegu)
Park, Mae-Ja (Department of Anatomy, School of Medicine, Kyungpook National University)
Paik, Sang-Kyoo (Department of Oral Anatomy, School of Dentistry, Kyungpook National University)
Moon, Che-Il (Department of Oral Anatomy, School of Dentistry, Kyungpook National University)
Kim, Yun-Sook (Department of Oral Anatomy, School of Dentistry, Kyungpook National University)
Bae, Yong-Chul (Department of Oral Anatomy, School of Dentistry, Kyungpook National University)
Publication Information
Applied Microscopy / v.38, no.3, 2008 , pp. 151-157 More about this Journal
Abstract
Trigeminal primary afferents expressing $P2X_3$ or transient receptor potential vanilloid 1 (TRPV1) are involved in the transmission of nociceptive information. In order to characterize $P2X_3$- and TRPV1-immunopositive neurons in the trigeminal ganglion (TG) and trigeminal caudal nucleus (Vc), we performed immunofluorescence experiments using anti-$P2X_3$ and anti-TRPV1 antisera and a morphometric analysis. 77.4% (1,401/1.801) of all the $P2X_3$-postive neurons coexpressed TRPV1 and 51.9% (1,401/2,698) of all the THFV1-immunopositive neurons also costained for $P2X_3$ in the TG. Immunoreactivity for both $P2X_3$ and TRPV1 were present in medium-sized neurons but not in small- and large-sized neurons. $P2X_3$ and/or TRPV1-immunopositive fibers were observed in the primary afferents and their associated axons in the Vc. These fibers and terminals were distributed in the superficial lamina of Vc: $P2X_3$-immunopositive fibers and terminals were distributed in the lamina I and II, expecially in the inner part of lamina II (lamina IIi), whereas TRPV1-immunopositive ones were densely detected in the lamina I and outer part of lamina II (lamina IIo). Immunopositive fibers and terminals for both $P2X_3$ and TRPV1 were observed on the border between lamina IIi and IIo. These results suggest that terminals coexpressing $P2X_3$ and TRPV1 are involved in specific roles in the transmission and processing of orofacial nociceptive information.
Keywords
$P2X_3$; TRPV1; Trigeminal ganglion; Trigeminal caudalis; Immunofluorescence;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Hamilton SG, Wade A, McMahon SB: The effects of inflammation and inflammatory mediators on nociceptive behaviour induced by ATP analogues in the rat. Br J Pharmacol 126 : 326-332, 1999   DOI   ScienceOn
2 Hwang IK, Lee HY, Yoo KY, Seong NS, Chung HG, Kim JH, Lee HJ, Lee WH, Kang TC, Won MH: Chronological alterations of $P2X_{3}$ receptor expression in the trigeminal ganglion after ischaemic insult in the Mongolian gerbil. Anat Histol Embryol 33 : 220-224, 2004   DOI   ScienceOn
3 Jiang J, Gu J: Expression of adenosine triphosphate $P2X_{3}$ receptors in rat molar pulp and trigeminal ganglia. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 94 : 622-626, 2002   DOI   ScienceOn
4 Kim YS, Paik SK, Cho YS, Shin HS, Bae JY, Moritani M, Yoshida A, Ahn DK, Valtschanoff J, Hwang SJ, Moon C, Bae YC: Expression of $P2X_{3}$ receptor in the trigeminal sensory nuclei of the rat. J Comp Neurol 506 : 627-39, 2008   DOI   ScienceOn
5 Sikand P, Premkumar LS: Potentiation of glutamatergic synaptic transmission by protein kinase C-mediated sensitization of TRPV1 at the first sensory synapse. J Physiol 581(Pt 2) : 631-647, 2007   DOI   ScienceOn
6 Burnstock G: A unifying purinergic hypothesis for the initiation of pain. Lancet 347 : 1604-1605, 1996   DOI   ScienceOn
7 Olszewski J: On the anatomical and functional organization of the spinal trigeminal nucleus. J Comp Neurol 92 : 401-413, 1950   DOI   ScienceOn
8 Burnstock G: P2X receptors in sensory neurones. Br J Anaesth 84 : 476-488, 2000   DOI   ScienceOn
9 Vulchanova L, Riedl MS, Shuster SJ, Buell G, Surprenant A, North RA, Elde R: Immunohistochemical study of the $P2X_{2}$ and $P2X_{3}$ receptor subunits in rat and monkey sensory neurons and their central terminals. Neuropharmacology 36 : 1229-1242, 1997   DOI   ScienceOn
10 Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H, Skinner K, Raumann BE, Basbaum AI, Julius D: The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21 : 531-543, 1998   DOI   ScienceOn
11 Eriksson J, Bongenhielm U, Kidd E, Matthews B, Fried K: Distribution of $P2X_{3}$ receptors in the rat trigeminal ganglion after inferior alveolar nerve injury. Neurosci Lett 254 : 37-40, 1998   DOI   ScienceOn
12 Guo A, Vulchanova L, Wang J, Li X, Elde R: Immunocytochemical localization of the vanilloid receptor 1 (VR1): relationship to neuropeptides, the P2X3 purinoceptor and IB4 binding sites. Eur J Neurosci 11 : 946-958, 1999   DOI   ScienceOn
13 Llewellyn-Smith IJ, Burnstock G: Ultrastructural localization of $P2X_{3}$ receptors in rat sensory neurons. Neuroreport 9 : 2545-2550, 1998   DOI   ScienceOn
14 Bradbury EJ, Burnstock G, McMahon SB: The expression of $P2X_{3}$ purinoreceptors in sensory neurons: effects of axotomy and glial-derived neurotrophic factor. Mol Cell Neurosci 12 : 256-268, 1998   DOI   ScienceOn
15 Hamilton SG, Warburton J, Bhattacharjee A, Ward J, McMahon SB: ATP in human skin elicits a dose-related pain response which is potentiated under conditions of hyperalgesia. Brain 123(Pt 6) : 1238-1246, 2000   DOI   ScienceOn
16 Le KT, Villeneuve P, Ramjaun AR, McPherson PS, Beaudet A, Seguela P: Sensory presynaptic and widespread somatodendritic immunolocalization of central ionotropic P2X ATP receptors. Neuroscience 83 : 177-190, 1998   DOI   ScienceOn
17 Driessen B, Reimann W, Selve N, Friderichs E, Bultmann R: Antinociceptive effect of intrathecally administered P2-purinoceptor antagonists in rats. Brain Res 666 : 182-188, 1994   DOI   ScienceOn
18 Helliwell RJ, McLatchie LM, Clarke M, Winter J, Bevan S, McIntyre P: Capsaicin sensitivity is associated with the expression of the vanilloid (capsaicin) receptor (VR1) mRNA in adult rat sensory ganglia. Neurosci Lett 250 : 177-180, 1998   DOI   ScienceOn
19 Szallasi A, Blumberg PM: Vanilloid (Capsaicin) receptors and mechanisms. Pharmacol Rev 51 : 159-212, 1999
20 Burnstock G: Local mechanisms of blood flow control by perivascular nerves and endothelium. J Hypertens Suppl 8 : S95-106, 1990   DOI
21 Ichikawa H, Sugimoto T: VR1-immunoreactive primary sensory neurons in the rat trigeminal ganglion. Brain Res 890 : 184-188, 2001   DOI   ScienceOn
22 Loesch A, Burnstock G: Electron-immunocytochemical localization of $P2X_{1}$ receptors in the rat cerebellum. Cell Tissue Res 294 : 253-260, 1998   DOI
23 Vulchanova L, Riedl MS, Shuster SJ, Stone LS, Hargreaves KM, Buell G, Surprenant A, North RA, Elde R: $P2X_{3}$ is expressed by DRG neurons that terminate in inner lamina II. Eur J Neurosci 10 : 3470-3478, 1998   DOI   ScienceOn
24 Aoki Y, Ohtori S, Takahashi K, Ino H, Ozawa T, Douya H, Chiba T, Moriya H: $P2X_{3}$-immunoreactive primary sensory neurons innervating lumbar intervertebral disc in rats. Brain Res 989 : 214-220, 2003   DOI   ScienceOn
25 Hwang SJ, Valtschanoff JG: Vanilloid receptor VR1-positive afferents are distributed differently at different levels of the rat lumbar spinal cord. Neurosci Lett 349 : 41-44, 2003   DOI   ScienceOn
26 Michael GJ, Priestley JV: Differential expression of the mRNA for the vanilloid receptor subtype 1 in cells of the adult rat dorsal root and nodose ganglia and its downregulation by axotomy. J Neurosci 19 : 1844-1854. 1999   DOI
27 Caterina MJ, Julius D: The vanilloid receptor: a molecular gateway to the pain pathway. Annu Rev Neurosci 24 : 487-517, 2001   DOI   ScienceOn
28 Xiang Z, Bo X, Burnstock G: Localization of ATP-gated P2X receptor immunoreactivity in rat sensory and sympathetic ganglia. Neurosci Lett 256 : 105-108, 1998   DOI   ScienceOn
29 Li P, Calejesan AA, Zhuo M: ATP P2X receptors and sensory synaptic transmission between primary afferent fibers and spinal dorsal horn neurons in rats. J Neurophysiol 80 : 3356-3360, 1998   DOI
30 Tsuda M, Ueno S, Inoue K: Evidence for the involvement of spinal endogenous ATP and P2X receptors in nociceptive responses caused by formalin and capsaicin in mice. Br J Pharmacol 128 : 1497-1504, 1999b   DOI   ScienceOn
31 Khakh BS, Henderson G: ATP receptor-mediated enhancement of fast excitatory neurotransmitter release in the brain. Mol Pharmacol 54 : 372-378, 1998   DOI
32 Siems WG, Grune T, Schmidt H, Tikhonov YV, Pimenov AM: Purine nucleotide levels in host tissues of Ehrlich ascites tumor-bearing mice in different growth phases of the tumor. Cancer Res 53 : 5143-5147, 1993
33 Tsuda M, Ueno S, Inoue K: In vivo pathway of thermal hyperalgesia by intrathecal administration of alpha,beta-methylene ATP in mouse spinal cord: involvement of the glutamate-NMDA receptor system. Br J Pharmacol 127 : 449-456, 1999a   DOI   ScienceOn
34 Valtschanoff JG, Rustioni A, Guo A, Hwang SJ: Vanilloid receptor VR1 is both presynaptic and postsynaptic in the superficial laminae of the rat dorsal horn. J Comp Neurol 436 : 225-235, 2001   DOI   ScienceOn
35 Collo G, North RA, Kawashima E, Merlo-Pich E, Neidhart S, Surprenant A, Buell G: Cloning OF $P2X_{5}$ and $P2X_{6}$ receptors and the distribution and properties of an extended family of ATPgated ion channels. J Neurosci 16 : 2495-2507, 1996   DOI
36 Ambalavanar R, Moritani M, Dessem D: Trigeminal $P2X_{3}$ receptor expression differs from dorsal root ganglion and is modulated by deep tissue inflammation. Pain 117 : 280-291, 2005   DOI   ScienceOn
37 Souslova V, Cesare P, Ding Y, Akopian AN, Stanfa L, Suzuki R, Carpenter K, Dickenson A, Boyce S, Hill R, Nebenuis-Oosthuizen D, Smith AJ, Kidd EJ, Wood JN: Warm-coding deficits and aberrant inflammatory pain in mice lacking $P2X_{3}$ receptors. Nature 407 : 1015-1017, 2000   DOI   ScienceOn
38 Cockayne DA, Hamilton SG, Zhu QM, Dunn PM, Zhong Y, Novakovic S, Malmberg AB, Cain G, Berson A, Kassotakis L, Hedley L, Lachnit WG, Burnstock G, McMahon SB, Ford AP: Urinary bladder hyporeflexia and reduced pain-related behaviour in $P2X_{3}$-deficient mice. Nature 407 : 1011-1015, 2000   DOI   ScienceOn
39 Coutts AA, Jorizzo JL, Eady RA, Greaves MW, Burnstock G: Adenosine triphosphate-evoked vascular changes in human skin: mechanism of action. Eur J Pharmacol 76 : 391-401, 1981   DOI   ScienceOn
40 Gu JG, MacDermott AB: Activation of ATP P2X receptors elicits glutamate release from sensory neuron synapses. Nature 389 : 749-753, 1997   DOI   ScienceOn
41 Novakovic SD, Kassotakis LC, Oglesby IB, Smith JA, Eglen RM, Ford AP, Hunter JC: Immunocytochemical localization of $P2X_{3}$ purinoceptors in sensory neurons in naive rats and following neuropathic injury. Pain 80 : 273-282, 1999   DOI   ScienceOn
42 Maehara Y, Kusumoto H, Anai H, Kusumoto T, Sugimachi K: Human tumor tissues have higher ATP contents than normal tissues. Clin Chim Acta 169 : 341-343, 1987   DOI   ScienceOn
43 Kanjhan R, Housley GD, Burton LD, Christie DL, Kippenberger A, Thorne PR, Luo L, Ryan AF: Distribution of the $P2X_{2}$ receptor subunit of the ATP-gated ion channels in the rat central nervous system. J Comp Neurol 407 : 11-32, 1999   DOI   ScienceOn