Skip to main content

Purines and Sensory Nerves

  • Chapter
  • First Online:
Sensory Nerves

Part of the book series: Handbook of Experimental Pharmacology ((HEP,volume 194))

Abstract

P2X and P2Y nucleotide receptors are described on sensory neurons and their peripheral and central terminals in dorsal root, nodose, trigeminal, petrosal, retinal and enteric ganglia. Peripheral terminals are activated by ATP released from local cells by mechanical deformation, hypoxia or various local agents in the carotid body, lung, gut, bladder, inner ear, eye, nasal organ, taste buds, skin, muscle and joints mediating reflex responses and nociception. Purinergic receptors on fibres in the dorsal spinal cord and brain stem are involved in reflex control of visceral and cardiovascular activity, as well as relaying nociceptive impulses to pain centres. Purinergic mechanisms are enhanced in inflammatory conditions and may be involved in migraine, pain, diseases of the special senses, bladder and gut, and the possibility that they are also implicated in arthritis, respiratory disorders and some central nervous system disorders is discussed. Finally, the development and evolution of purinergic sensory mechanisms are considered.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 429.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 549.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 549.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abbracchio MP, Burnstock G, Boeynaems J-M, Barnard EA, Boyer JL, Kennedy C, Knight GE, Fumagalli M, Gachet C, Jacobson KA, Weisman GA (2006) International Union of Pharmacology. Update and subclassification of the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy. Pharmacol Rev 58:281–341

    PubMed  CAS  Google Scholar 

  • Adriaensen D, Timmermans JP (2004) Purinergic signalling in the lung: important in asthma and COPD? Curr Opin Pharmacol 4:207–214

    PubMed  CAS  Google Scholar 

  • Adriaensen D, Brouns I, Pintelon I, De Proost I, Timmermans JP (2006) Evidence for a role of neuroepithelial bodies as complex airway sensors: comparison with smooth muscle-associated airway receptors. J Appl Physiol 101:960–970

    PubMed  CAS  Google Scholar 

  • Agboh KC, Webb TE, Evans RJ, Ennion SJ (2004) Functional characterization of a P2X receptor from Schistosoma mansoni. J Biol Chem 279:41650–41657

    PubMed  CAS  Google Scholar 

  • Alavi AM, Dubyak GR, Burnstock G (2001) Immunohistochemical evidence for ATP receptors in human dental pulp. J Dental Res 80:476–483

    CAS  Google Scholar 

  • Alcayaga C, Varas R, Valdes V, Cerpa V, Arroyo J, Iturriaga R, Alcayaga J (2007) ATP- and ACh-induced responses in isolated cat petrosal ganglion neurons. Brain Res 1131:60–67

    PubMed  CAS  Google Scholar 

  • Andersson KE, Wein AJ (2004) Pharmacology of the lower urinary tract: basis for current and future treatments of urinary incontinence. Pharmacol Rev 56:581–631

    PubMed  CAS  Google Scholar 

  • Antunes VR, Bonagamba LG, Machado BH (2005) Hemodynamic and respiratory responses to microinjection of ATP into the intermediate and caudal NTS of awake rats. Brain Res 1032:85–93

    PubMed  CAS  Google Scholar 

  • Aoki Y, Ohtori S, Takahashi K, Ino H, Ozawa T, Douya H, Chiba T, Moriya H (2003) P2X3-immunoreactive primary sensory neurons innervating lumbar intervertebral disc in rats. Brain Res 989:214–220

    PubMed  CAS  Google Scholar 

  • Apostolidis A, Popat R, Yiangou Y, Cockayne D, Ford AP, Davis JB, Dasgupta P, Fowler CJ, Anand P (2005) Decreased sensory receptors P2X3 and TRPV1 in suburothelial nerve fibers following intradetrusor injections of botulinum toxin for human detrusor overactivity. J Urol 174:977–982

    PubMed  CAS  Google Scholar 

  • Arthur DB, Akassoglou K, Insel PA (2005) P2Y2 receptor activates nerve growth factor/TrkA signaling to enhance neuronal differentiation. Proc Natl Acad Sci USA 102:19138–19143

    PubMed  CAS  Google Scholar 

  • Atiemo H, Wynes J, Chuo J, Nipkow L, Sklar GN, Chai TC (2005) Effect of botulinum toxin on detrusor overactivity induced by intravesical adenosine triphosphate and capsaicin in a rat model. Urology 65:622–626

    PubMed  Google Scholar 

  • Bartel DL, Sullivan SL, Lavoie EG, Sévigny J, Finger TE (2006) Nucleoside triphosphate diphosphohydrolase-2 is the ecto-ATPase of type I cells in taste buds. J Comp Neurol 497:1–12

    PubMed  CAS  Google Scholar 

  • Bertrand PP (2003) ATP and sensory transduction in the enteric nervous system. Neuroscientist 9:243–260

    Google Scholar 

  • Bertrand PP, Bornstein JC (2002) ATP as a putative sensory mediator: activation of intrinsic sensory neurons of the myenteric plexus via P2X receptors. J Neurosci 22:4767–4775

    Google Scholar 

  • Bian X, Ren J, DeVries M, Schnegelsberg B, Cockayne DA, Ford AP, Galligan JJ (2003) Peristalsis is impaired in the small intestine of mice lacking the P2X3 subunit. J Physiol 551:309–322

    PubMed  CAS  Google Scholar 

  • Birder LA (2006) Urinary bladder urothelium: molecular sensors of chemical/thermal/mechanical stimuli. Vasc Pharmacol 45:221–226

    CAS  Google Scholar 

  • Birder LA, Ruan HZ, Chopra B, Xiang Z, Barrick S, Buffington CA, Roppolo JR, Ford AP, de Groat WC, Burnstock G (2004) Alterations in P2X and P2Y purinergic receptor expression in urinary bladder from normal cats and cats with interstitial cystitis. Am J Physiol Renal Physiol 287:F1084–F1091

    PubMed  CAS  Google Scholar 

  • Blackshaw LA, Brookes SJ, Grundy D, Schemann M (2007) Sensory transmission in the gastrointestinal tract. Neurogastroenterol Motil 19:1–19

    PubMed  CAS  Google Scholar 

  • Bleehen T, Keele CA (1977) Observations on the algogenic actions of adenosine compounds on human blister base preparation. Pain 3:367–377

    PubMed  CAS  Google Scholar 

  • Bo X, Alavi A, Xiang Z, Oglesby I, Ford A, Burnstock G (1999) Localization of ATP-gated P2X2 and P2X3 receptor immunoreactive nerves in rat taste buds. Neuroreport 10:1107–1111

    PubMed  CAS  Google Scholar 

  • Bodin P, Burnstock G (2001) Purinergic signalling: ATP release. Neurochem Res 26:959–969

    PubMed  CAS  Google Scholar 

  • Borvendeg SJ, Al Khrasani M, Rubini P, Fischer W, Allgaier C, Wirkner K, Himmel HM, Gillen C, Illes P (2003) Subsensitivity of P2X but not vanilloid 1 receptors in dorsal root ganglia of rats caused by cyclophosphamide cystitis. Eur J Pharmacol 474:71–75

    PubMed  CAS  Google Scholar 

  • Bradbury EJ, Burnstock G, McMahon SB (1998) The expression of P2X3 purinoceptors in sensory neurons: effects of axotomy and glial-derived neurotrophic factor. Mol Cell Neurosci 12:256–268

    PubMed  CAS  Google Scholar 

  • Brady CM, Apostolidis A, Yiangou Y, Baecker PA, Ford AP, Freeman A, Jacques TS, Fowler CJ, Anand P (2004) P2X3-immunoreactive nerve fibres in neurogenic detrusor overactivity and the effect of intravesical resiniferatoxin. Eur Urol 46:247–253

    PubMed  CAS  Google Scholar 

  • Braga VA, Soriano RN, Braccialli AL, de Paula PM, Bonagamba LG, Paton JF, Machado BH (2007) Involvement of L-glutamate and ATP in the neurotransmission of the sympathoexcitatory component of the chemoreflex in the commissural nucleus tractus solitarii of awake rats and in the working heart-brainstem preparation. J Physiol 581:1129–1145

    PubMed  CAS  Google Scholar 

  • Brierley SM, Carter R, Jones W III, Xu L, Robinson DR, Hicks GA, Gebhart GF, Blackshaw LA (2005) Differential chemosensory function and receptor expression of splanchnic and pelvic colonic afferents in mice. J Physiol 567:267–281

    PubMed  CAS  Google Scholar 

  • Brouns I, Van Genechten J, Burnstock G, Timmermans J-P, Adriaensen D (2003) Ontogenesis of P2X3 receptor-expressing nerve fibres in the rat lung, with special reference to neuroepithelial bodies. Biomed Res 14:80–86

    CAS  Google Scholar 

  • Brouns I, Pintelon I, De Proost I, Alewaters R, Timmermans JP, Adriaensen D (2006) Neurochemical characterisation of sensory receptors in airway smooth muscle: comparison with pulmonary neuroepithelial bodies. Histochem Cell Biol 125:351–367

    PubMed  CAS  Google Scholar 

  • Burnstock G (1981) Pathophysiology of migraine: a new hypothesis. Lancet 317:1397–1399

    Google Scholar 

  • Burnstock G (1989) The role of adenosine triphosphate in migraine. Biomed Pharmacother 43:727–736

    PubMed  CAS  Google Scholar 

  • Burnstock G (1993) Introduction: changing face of autonomic and sensory nerves in the circulation. In: Edvinsson L, Uddman R (eds) Vascular innervation and receptor mechanisms: new perspectives. Academic, San Diego, pp 1–22

    Google Scholar 

  • Burnstock G (1996a) Purinoceptors: ontogeny and phylogeny. Drug Dev Res 39:204–242

    CAS  Google Scholar 

  • Burnstock G (1996b) A unifying purinergic hypothesis for the initiation of pain. Lancet 347:1604–1605

    PubMed  CAS  Google Scholar 

  • Burnstock G (1999) Release of vasoactive substances from endothelial cells by shear stress and purinergic mechanosensory transduction. J Anat 194:335–342

    PubMed  CAS  Google Scholar 

  • Burnstock G (2000) P2X receptors in sensory neurones. Br J Anaesth 84:476–488

    PubMed  CAS  Google Scholar 

  • Burnstock G (2001a) Purine-mediated signalling in pain and visceral perception. Trends Pharmacol Sci 22:182–188

    PubMed  CAS  Google Scholar 

  • Burnstock G (2001b) Purinergic signalling in development. In: Abbracchio MP, Williams M (eds) Purinergic and pyrimidinergic signalling I – molecular, nervous and urinogenitary system function. Handbook of experimental pharmacology, vol 151/I. Springer, Berlin, pp 89–127

    Google Scholar 

  • Burnstock G (2003) Purinergic receptors in the nervous system. In: Schwiebert EM (ed) Purinergic receptors and signalling. Current topics in membranes, vol 54. Academic, San Diego, pp 307–368

    Google Scholar 

  • Burnstock G (2006) Purinergic P2 receptors as targets for novel analgesics. Pharmacol Therap 110:433–454

    CAS  Google Scholar 

  • Burnstock G (2007) Physiology and pathophysiology of purinergic neurotransmission. Physiol Rev 87:659–797

    PubMed  CAS  Google Scholar 

  • Burnstock G, Knight GE (2004) Cellular distribution and functions of P2 receptor subtypes in different systems. Int Rev Cytol 240:31–304

    PubMed  CAS  Google Scholar 

  • Burnstock G, Wood JN (1996) Purinergic receptors: their role in nociception and primary afferent neurotransmission. Curr Opin Neurobiol 6:526–532

    PubMed  CAS  Google Scholar 

  • Bystrova MF, Yatzenko YE, Fedorov IV, Rogachevskaja OA, Kolesnikov SS (2006) P2Y isoforms operative in mouse taste cells. Cell Tissue Res 323:377–382

    PubMed  CAS  Google Scholar 

  • Cao Y, Song G (2007) Purinergic modulation of respiration via medullary raphe nuclei in rats. Respir Physiol Neurobiol 155:114–120

    PubMed  CAS  Google Scholar 

  • Cao Y, Lai W-L, Chen Y-X (2006) Differential regulation of P2X3 protein expression in the rat trigeminal ganglion after experimental tooth movement. West China J Stomatol 24:389–392

    CAS  Google Scholar 

  • Castelucci P, Robbins HL, Furness JB (2003) P2X2 purine receptor immunoreactivity of intraganglionic laminar endings in the mouse gastrointestinal tract. Cell Tissue Res 312:167–174

    PubMed  CAS  Google Scholar 

  • Ceruti C, Fumagalli M, Verderio C, Abbracchio MP (2006) Nucleotides as neurotransmitters of pain in migraine: a role for P2Y receptors in primary cultures from mouse trigeminal ganglia. In: Proceedings of the American Society for Neuroscience, Atlanta, GA, 14-18 October 2006

    Google Scholar 

  • Chan ESL, Fernandez P, Cronstein BN (2007) Adenosine in inflammatory joint diseases. Purinergic Signal 3:145–152

    PubMed  CAS  Google Scholar 

  • Chen C, Nenov A, Bobbin RP (1995a) Noise exposure alters the response of outer hair cells to ATP. Hear Res 88:215–221

    PubMed  CAS  Google Scholar 

  • Chen CC, Akopian AN, Sivilotti L, Colquhoun D, Burnstock G, Wood JN (1995b) A P2X purinoceptor expressed by a subset of sensory neurons. Nature 377:428–431

    PubMed  CAS  Google Scholar 

  • Chen CL, Broom DC, Liu Y, de Nooij JC, Li Z, Cen C, Samad OA, Jessell TM, Woolf CJ, Ma Q (2006) Runx1 determines nociceptive sensory neuron phenotype and is required for thermal and neuropathic pain. Neuron 49:365–377

    PubMed  CAS  Google Scholar 

  • Chessell IP, Hatcher JP, Hughes JP, Ulmann L, Green P, Mander PK, Reeve AJ, Rassendren F (2006) The role of P2X7 and P2X4 in pain processing; common or divergent pathways? Purinergic Signal 2:46–47

    Google Scholar 

  • Cheung K-K, Burnstock G (2002) Localisation of P2X3 and co-expression with P2X2 receptors during rat embryonic neurogenesis. J Comp Neurol 443:368–382

    PubMed  CAS  Google Scholar 

  • Cockayne DA, Hamilton SG, Zhu Q-M, Dunn PM, Zhong Y, Novakovic S, Malmberg AB, Cain G, Berson A, Kassotakis L, Hedley L, Lachnit WG, Burnstock G, McMahon SB, Ford APDW (2000) Urinary bladder hyporeflexia and reduced pain-related behaviour in P2X3-deficient mice. Nature 407:1011–1015

    PubMed  CAS  Google Scholar 

  • Cockayne DA, Dunn PM, Zhong Y, Hamilton SG, Cain GR, Knight GE, Ruan H-Z, Ping Y, Nunn P, Bei M, McMahon SB, Burnstock G, Ford APDW (2005) P2X2 knockout mice and P2X2/P2X3 double knockout mice reveal a role for the P2X2 receptor subunit in mediating multiple sensory effects of ATP. J Physiol 567:621–639

    PubMed  CAS  Google Scholar 

  • Collier HO, James GWL, Schneider C (1966) Antagonism by aspirin and fenamates of bronchoconstriction and nociception induced by adenosine-5′-triphosphate. Nature 212:411–412

    PubMed  CAS  Google Scholar 

  • Cook SP, McCleskey EW (2002) Cell damage excites nociceptors through release of cytosolic ATP. Pain 95:41–47

    PubMed  CAS  Google Scholar 

  • Cooke HJ, Wunderlich J, Christofi FL (2003) “The force be with you”: ATP in gut mechanosensory transduction. News Physiol Sci 18:43–49

    PubMed  CAS  Google Scholar 

  • Damann N, Rothermel M, Klupp BG, Mettenleiter TC, Hatt H, Wetzel CH (2006) Chemosensory properties of murine nasal and cutaneous trigeminal neurons identified by viral tracing. BMC Neurosci 7:46

    PubMed  Google Scholar 

  • Dang K, Bielefeldt K, Gebhart GF (2004) Distinct P2X receptors on thoracolumbar and lumbosacral dorsal root ganglion neurons innervating the rat urinary bladder. Abstract viewer/itinerary planner. Program no. 2856.1 2004. Society for Neuroscience, Washington

    Google Scholar 

  • Dang K, Bielfeldt K, Lamb K, Gebhart GF (2005) Gastric ulcers evoke hyperexcitability and enhance P2X receptor function in rat gastric sensory neurons. J Neurophysiol 93:3112–3119

    PubMed  CAS  Google Scholar 

  • Davies DL, Kochegarov AA, Kuo ST, Kulkarni AA, Woodward JJ, King BF, Alkana RL (2005) Ethanol differentially affects ATP-gated P2X3 and P2X4 receptor subtypes expressed in Xenopus oocytes. Neuropharmacology 49:243–253

    PubMed  CAS  Google Scholar 

  • de Groat WC (2006) Integrative control of the lower urinary tract: preclinical perspective. Br J Pharmacol 147:S25–S40

    PubMed  CAS  Google Scholar 

  • Dell'Antonio G, Quattrini A, Cin ED, Fulgenzi A, Ferrero ME (2002) Relief of inflammatory pain in rats by local use of the selective P2X7 ATP receptor inhibitor, oxidized ATP. Arthritis Rheumatism 46:3378–3385

    PubMed  Google Scholar 

  • Denda M, Nakatani M, Ikeyama K, Tsutsumi M, Denda S (2007) Epidermal keratinocytes as the forefront of the sensory system. Exp Dermatol 16:157–161

    PubMed  CAS  Google Scholar 

  • Dorn G, Patel S, Wotherspoon G, Hemmings-Mieszczak M, Barclay J, Natt FJ, Martin P, Bevan S, Fox A, Ganju P, Wishart W, Hall J (2004) siRNA relieves chronic neuropathic pain. Nucleic Acids Res 32:e49

    PubMed  Google Scholar 

  • Dowd E, McQueen DS, Chessell IP, Humphrey PPA (1998) P2X receptor-mediated excitation of nociceptive afferents in the normal and arthritic rat knee joint. Br J Pharmacol 125:341–346

    PubMed  CAS  Google Scholar 

  • Du S, Araki I, Mikami Y, Zakoji H, Beppu M, Yoshiyama M, Takeda M (2007) Amiloride-sensitive ion channels in urinary bladder epithelium involved in mechanosensory transduction by modulating stretch-evoked adenosine triphosphate release. Urology 69:590–595

    PubMed  Google Scholar 

  • Dulon D, Jagger DJ, Lin X, Davis RL (2006) Neuromodulation in the spiral ganglion: shaping signals from the organ of corti to the CNS. J Membr Biol 209:167–175

    PubMed  CAS  Google Scholar 

  • Dunn PM, Zhong Y, Burnstock G (2001) P2X receptors in peripheral neurones. Prog Neurobiol 65:107–134

    PubMed  CAS  Google Scholar 

  • Färber K, Kettenmann H (2006) Purinergic signaling and microglia. Pflugers Arch Eur J Physiol 452:615–621

    Google Scholar 

  • Ferrari D, Pizzirani C, Adinolfi E, Lemoli RM, Curti A, Idzko M, Panther E, Di Virgilio F (2006) The P2X7 receptor: a key player in IL-1 processing and release. J Immunol 176:3877–3883

    PubMed  CAS  Google Scholar 

  • Finger TE, Danilova V, Barrows J, Bartel DL, Vigers AJ, Stone L, Hellekant G, Kinnamon SC (2005) ATP signaling is crucial for communication from taste buds to gustatory nerves. Science 310:1495–1499

    PubMed  CAS  Google Scholar 

  • Ford AP, Gever JR, Nunn PA, Zhong Y, Cefalu JS, Dillon MP, Cockayne DA (2006) Purinoceptors as therapeutic targets for lower urinary tract dysfunction. Br J Pharmacol 147:S132–S143

    PubMed  CAS  Google Scholar 

  • Fountain SJ, Parkinson K, Young MT, Cao L, Thompson CR, North RA (2007) An intracellular P2X receptor required for osmoregulation in Dictyostelium discoideum. Nature 448:200–203

    PubMed  CAS  Google Scholar 

  • Frohlich R, Boehm S, Illes P (1996) Pharmacological characterization of P2 purinoceptor types in rat locus coeruleus neurons. Eur J Pharmacol 315:255–261

    PubMed  CAS  Google Scholar 

  • Fukui M, Nakagawa T, Minami M, Satoh M, Kaneko S (2006) Inhibitory role of supraspinal P2X3/P2X2/3 subtypes on nociception in rats. Mol Pain 2:19–25

    PubMed  Google Scholar 

  • Fumagalli M, Ceruti S, Verderio C, Abbracchio MP (2006) ATP as a neurotransmitter of pain in migraine: a functional role for P2Y receptors in primary cultures from mouse trigeminal sensory ganglia. Purinergic Signal 2:120–121

    Google Scholar 

  • Furness JB, Kunze WA, Bertrand PP, Clerc N, Bornstein JC (1998) Intrinsic primary afferent neurons of the intestine. Prog Neurobiol 54:1–18

    PubMed  CAS  Google Scholar 

  • Fyffe REW, Perl ER (1984) Is ATP a central synaptic mediator for certain primary afferent fibres from mammalian skin? Proc Natl Acad Sci USA 81:6890–6893

    PubMed  CAS  Google Scholar 

  • Gale JE, Piazza V, Ciubotaru CD, Mammano F (2004) A mechanism for sensing noise damage in the inner ear. Curr Biol 14:526–529

    PubMed  CAS  Google Scholar 

  • Galligan JJ (2004) Enteric P2X receptors as potential targets for drug treatment of the irritable bowel syndrome. Br J Pharmacol 141:1294–1302

    PubMed  CAS  Google Scholar 

  • Gao Z, Kehoe V, Sinoway LI, Li J (2005) Spinal P2X receptor modulates reflex pressor response to activation of muscle afferents. Am J Physiol Heart Circ Physiol 288:H2238–H2243

    PubMed  CAS  Google Scholar 

  • Gao N, Hu HZ, Zhu MX, Fang X, Liu S, Gao C, Wood JD (2006) The P2Y1 purinergic receptor expressed by enteric neurones in guinea-pig intestine. Neurogastroenterol Motil 18:316–323

    PubMed  CAS  Google Scholar 

  • Gayle S, Burnstock G (2005) Immunolocalisation of P2X and P2Y nucleotide receptors in the rat nasal mucosa. Cell Tissue Res 319:27–36

    PubMed  CAS  Google Scholar 

  • Gerevich Z, Zadori Z, Müller C, Wirkner K, Schröder W, Rubini P, Illes P (2007) Metabotropic P2Y receptors inhibit P2X3 receptor-channels via G protein-dependent facilitation of their desensitization. Br J Pharmacol 151:226–236

    PubMed  CAS  Google Scholar 

  • Gever J, Cockayne DA, Dillon MP, Burnstock G, Ford APDW (2006) Pharmacology of P2X channels. Pflugers Arch Eur J Physiol 452:513–537

    CAS  Google Scholar 

  • Gilchrist LS, Cain DM, Harding-Rose C, Kov AN, Wendelschafer-Crabb G, Kennedy WR, Simone DA (2005) Re-organization of P2X3 receptor localization on epidermal nerve fibers in a murine model of cancer pain. Brain Res 1044:197–205

    PubMed  CAS  Google Scholar 

  • Goadsby PJ (2005) Migraine, allodynia, sensitisation and all of that. Eur Neurol 53:10–16

    PubMed  Google Scholar 

  • Gourine AV (2005) On the peripheral and central chemoreception and control of breathing: an emerging role of ATP. J Physiol 568:715–724

    PubMed  CAS  Google Scholar 

  • Gourine AV, Melenchuk EV, Poputnikov DM, Gourine VN, Spyer KM (2002) Involvement of purinergic signalling in central mechanisms of body temperature regulation in rats. Br J Pharmacol 135:2047–2055

    PubMed  CAS  Google Scholar 

  • Gourine AV, Atkinson L, Deuchars J, Spyer KM (2003) Purinergic signalling in the medullary mechanisms of respiratory control in the rat: respiratory neurones express the P2X2 receptor subunit. J Physiol 552:197–211

    PubMed  CAS  Google Scholar 

  • Gourine AV, Dale N, Gourine VN, Spyer KM (2004) Fever in systemic inflammation: roles of purines. Front Biosci 9:1011–1022

    PubMed  CAS  Google Scholar 

  • Green PG, Basbaum AI, Helms C, Levine JD (1991) Purinergic regulation of bradykinin-induced plasma extravasation and adjuvant-induced arthritis in the rat. Proc Natl Acad Sci USA 88:4162–4165

    PubMed  CAS  Google Scholar 

  • Greenwood D, Jagger DJ, Huang LC, Hoya N, Thorne PR, Wildman SS, King BF, Pak K, Ryan AF, Housley GD (2007) P2X receptor signaling inhibits BDNF-mediated spiral ganglion neuron development in the neonatal rat cochlea. Development 134:1407–1417

    PubMed  CAS  Google Scholar 

  • Groenewegen HJ, Uylings HB (2000) The prefrontal cortex and the integration of sensory, limbic and autonomic information. Prog Brain Res 126:3–28

    PubMed  CAS  Google Scholar 

  • Gu YZ, Yin GF, Guan BC, Li ZW (2006) Characteristics of P2X purinoceptors in the membrane of rat trigeminal ganglion neurons. Sheng Li Xue Bao 58:164–170

    PubMed  CAS  Google Scholar 

  • Hamilton SG, McMahon SB, Lewin GR (2001) Selective activation of nociceptors by P2X receptor agonists in normal and inflamed rat skin. J Physiol 534:437–445

    PubMed  CAS  Google Scholar 

  • Harms L, Finta EP, Tschöpl M, Illes P (1992) Depolarization of rat locus coeruleus neurons by adenosine 5′-triphosphate. Neuroscience 48:941–952

    PubMed  CAS  Google Scholar 

  • He L, Chen J, Dinger B, Stensaas L, Fidone S (2006) Effect of chronic hypoxia on purinergic synaptic transmission in rat carotid body. J Appl Physiol 100:157–162

    PubMed  CAS  Google Scholar 

  • Hegg CC, Lucero MT (2006) Purinergic receptor antagonists inhibit odorant-induced heat shock protein 25 induction in mouse olfactory epithelium. Glia 53:182–190

    PubMed  Google Scholar 

  • Hegg CC, Greenwood D, Huang W, Han P, Lucero MT (2003) Activation of purinergic receptor subtypes modulates odor sensitivity. J Neurosci 23:8291–8301

    PubMed  CAS  Google Scholar 

  • Hemmings-Mieszczak M, Dorn G, Natt FJ, Hall J, Wishart WL (2003) Independent combinatorial effect of antisense oligonucleotides and RNAi-mediated specific inhibition of the recombinant rat P2X3 receptor. Nucleic Acids Res 31:2117–2126

    PubMed  CAS  Google Scholar 

  • Holton P (1959) The liberation of adenosine triphosphate on antidromic stimulation of sensory nerves. J Physiol (Lond) 145:494–504

    CAS  Google Scholar 

  • Holzer P (2004) Gastrointestinal pain in functional bowel disorders: sensory neurons as novel drug targets. Expert Opin Ther Targets 8:107–123

    PubMed  CAS  Google Scholar 

  • Holzer P (2007) Taste receptors in the gastrointestinal tract. V. Acid sensing in the gastrointestinal tract. Am J Physiol Gastrointest Liver Physiol 292:G699–G705

    Google Scholar 

  • Honore P, Donnelly-Roberts D, Namovic MT, Hsieh G, Zhu CZ, Mikusa JP, Hernandez G, Zhong C, Gauvin DM, Chandran P, Harris R, Medrano AP, Carroll W, Marsh K, Sullivan JP, Faltynek CR, Jarvis MF (2006) A-740003 [N-(1-{[(cyanoimino)(5-quinolinylamino) methyl]amino}-2,2-dimethylpropyl)-2-(3,4-dimethoxyphenyl)acetamide], a novel and selective P2X7 receptor antagonist, dose-dependently reduces neuropathic pain in the rat. J Pharmacol Exp Ther 319:1376–1385

    PubMed  CAS  Google Scholar 

  • Housley GD, Marcotti W, Navaratnam D, Yamoah EN (2006) Hair cells – beyond the transducer. J Membr Biol 209:89–118

    PubMed  CAS  Google Scholar 

  • Hu B, Chiang CY, Hu JW, Dostrovsky JO, Sessle BJ (2002) P2X receptors in trigeminal subnucleus caudalis modulate central sensitization in trigeminal subnucleus oralis. J Neurophysiol 88:1614–1624

    PubMed  CAS  Google Scholar 

  • Hu ST, Gever J, Nunn PA, Ford AP, Zhu Q-M (2004) Cystometric studies with ATP, PPADS and TNP-ATP in conscious and anaesthetised C57BL/6 mice. J Urol 171:461–462

    Google Scholar 

  • Huang LC, Ryan AF, Cockayne DA, Housley GD (2006) Developmentally regulated expression of the P2X3 receptor in the mouse cochlea. Histochem Cell Biol 125:681–692

    PubMed  CAS  Google Scholar 

  • Huang YJ, Maruyama Y, Dvoryanchikov G, Pereira E, Chaudhari N, Roper SD (2007) The role of pannexin 1 hemichannels in ATP release and cell-cell communication in mouse taste buds. Proc Natl Acad Sci USA 104:6436–6441

    PubMed  CAS  Google Scholar 

  • Hughes JP, Hatcher JP, Chessell IP (2007) The role of P2X7 in pain and inflammation. Purinergic Signal 3:163–169

    PubMed  CAS  Google Scholar 

  • Ichikawa H, Fukunaga T, Jin HW, Fujita M, Takano-Yamamoto T, Sugimoto T (2004) VR1-, VRL-1- and P2X3 receptor-immunoreactive innervation of the rat temporomandibular joint. Brain Res 1008:131–136

    PubMed  CAS  Google Scholar 

  • Ichikawa H, De Repentigny Y, Kothary R, Sugimoto T (2006) The survival of vagal and glossopharyngeal sensory neurons is dependent upon dystonin. Neuroscience 137:531–536

    PubMed  CAS  Google Scholar 

  • Ikeda H, Tsuda M, Inoue K, Murase K (2007) Long-term potentiation of neuronal excitation by neuron-glia interactions in the rat spinal dorsal horn. Eur J Neurosci 25:1297–1306

    PubMed  Google Scholar 

  • Inoue K (2007) P2 receptors and chronic pain. Purinergic Signal 3:135–144

    PubMed  CAS  Google Scholar 

  • Jahr CE, Jessell TM (1983) ATP excites a subpopulation of rat dorsal horn neurones. Nature 304:730–733

    PubMed  CAS  Google Scholar 

  • Jennings EA, Christie MJ, Sessle BJ (2006) ATP potentiates neurotransmission in the rat trigeminal subnucleus caudalis. Neuroreport 17:1507–1510

    PubMed  CAS  Google Scholar 

  • Kamei J, Takahashi Y, Yoshikawa Y, Saitoh A (2005) Involvement of P2X receptor subtypes in ATP-induced enhancement of the cough reflex sensitivity. Eur J Pharmacol 528:158–161

    PubMed  CAS  Google Scholar 

  • Kataoka S, Toyono T, Seta Y, Ogura T, Toyoshima K (2004) Expression of P2Y1 receptors in rat taste buds. Histochem Cell Biol 121:419–426

    PubMed  CAS  Google Scholar 

  • Kindig AE, Hayes SG, Kaufman MP (2007) Purinergic 2 receptor blockade prevents the responses of group IV afferents to post-contraction circulatory occlusion. J Physiol 578:301–308

    PubMed  CAS  Google Scholar 

  • King BF, Knowles I, Burnstock G, Ramage A (2004) Investigation of the effects of P2 purinoceptor ligands on the micturition reflex in female urethane-anaesthetised rats. Br J Pharmacol 142:519–530

    PubMed  CAS  Google Scholar 

  • Kitchen AM, Collins HL, DiCarlo SE, Scislo TJ, O'Leary DS (2001) Mechanisms mediating NTS P2x receptor-evoked hypotension: cardiac output vs. total peripheral resistance. Am J Physiol Heart Circ Physiol 281:H2198–H2203

    PubMed  CAS  Google Scholar 

  • Knight GE, Bodin P, de Groat WC, Burnstock G (2002) ATP is released from guinea pig ureter epithelium on distension. Am J Physiol Renal Physiol 282:F281–F288

    PubMed  CAS  Google Scholar 

  • Kobayashi K, Fukuoka T, Yamanaka H, Dai Y, Obata K, Tokunaga A, Noguchi K (2006) Neurons and glial cells differentially express P2Y receptor mRNAs in the rat dorsal root ganglion and spinal cord. J Comp Neurol 498:443–454

    PubMed  CAS  Google Scholar 

  • Koizumi S, Fujishita K, Inoue K, Shigemoto-Mogami Y, Tsuda M, Inoue K (2004) Ca2+ waves in keratinocytes are transmitted to sensory neurons: the involvement of extracellular ATP and P2Y2 receptor activation. Biochem J 380:329–338

    PubMed  CAS  Google Scholar 

  • Kollarik M, Dinh QT, Fischer A, Undem BJ (2003) Capsaicin-sensitive and -insensitive vagal bronchopulmonary C-fibres in the mouse. J Physiol 551:869–879

    PubMed  CAS  Google Scholar 

  • Kollarik M, Ru F, Undem BJ (2007) Acid-sensitive vagal sensory pathways and cough. Pulm Pharmacol Ther 20:402–411

    PubMed  CAS  Google Scholar 

  • Korim WS, Ferreira-Neto ML, Cravo SLD (2007) Role of NTS P2x receptors in cardiovascular adjustments during alerting defense reactions. FASEB J 21:5750.16

    Google Scholar 

  • Krishtal OA, Marchenko SM, Pidoplichko VI (1983) Receptor for ATP in the membrane of mammalian sensory neurones. Neurosci Lett 35:41–45

    PubMed  CAS  Google Scholar 

  • Krishtal O, Lozovaya N, Fedorenko A, Savelyev I, Chizhmakov I (2006) The agonists for nociceptors are ubiquitous, but the modulators are specific: P2X receptors in the sensory neurons are modulated by cannabinoids. Pflugers Arch Eur J Physiol 453:353–360

    CAS  Google Scholar 

  • Labrakakis C, Gerstner E, MacDermott AB (2000) Adenosine triphosphate-evoked currents in cultured dorsal root ganglion neurons obtained from rat embryos: desensitization kinetics and modulation of glutamate release. Neuroscience 101:1117–1126

    PubMed  CAS  Google Scholar 

  • Lahiri S, Mitchell CH, Reigada D, Roy A, Cherniack NS (2007) Purines, the carotid body and respiration. Respir Physiol Neurobiol 157:123–129

    PubMed  CAS  Google Scholar 

  • Lazarowski ER, Boucher RC, Harden TK (2003) Mechanisms of release of nucleotides and integration of their action as P2X- and P2Y-receptor activating molecules. Mol Pharmacol 64:785–795

    PubMed  CAS  Google Scholar 

  • Lee JH, Heo JH, Kim CH, Chang SO, Kim CS, Oh SH (2007) Changes in P2Y4 receptor expression in rat cochlear outer sulcus cells during development. Hear Res 228:201–211

    PubMed  CAS  Google Scholar 

  • Lewis C, Neidhart S, Holy C, North RA, Buell G, Surprenant A (1995) Coexpression of P2X2 and P2X3 receptor subunits can account for ATP-gated currents in sensory neurons. Nature 377:432–435

    PubMed  CAS  Google Scholar 

  • Li P, Calejesan AA, Zhou M (1998) ATP P2X receptors and sensory synaptic transmission between primary afferent fibers and spinal dorsal horn neurons in rats. J Neurophysiol 80:3356–3360

    PubMed  CAS  Google Scholar 

  • Lin JH, Takano T, Arcuino G, Wang X, Hu F, Darzynkiewicz Z, Nunes M, Goldman SA, Nedergaard M (2007) Purinergic signaling regulates neural progenitor cell expansion and neurogenesis. Dev Biol 302:356–366

    PubMed  CAS  Google Scholar 

  • Llewellyn-Smith IJ, Burnstock G (1998) Ultrastructural localization of P2X3 receptors in rat sensory neurons. Neuroreport 9:2245–2250

    Google Scholar 

  • Loesch A, Burnstock G (2001) Immunoreactivity to P2X6 receptors in the rat hypothalamo-neurohypophysial system: an ultrastructural study with ExtrAvidin and colloidal gold-silver immunolabelling. Neuroscience 106:621–631

    PubMed  CAS  Google Scholar 

  • Loredo GA, Benton HP (1998) ATP and UTP activate calcium-mobilizing P2U-like receptors and act synergistically with interleukin-1 to stimulate prostaglandin E2 release from human rheumatoid synovial cells. Arthritis Rheumatism 41:246–255

    PubMed  CAS  Google Scholar 

  • Lorier AR, Huxtable AG, Robinson DM, Lipski J, Housley GD, Funk GD (2007) P2Y1 receptor modulation of the pre-Bötzinger complex inspiratory rhythm generating network in vitro. J Neurosci 27:993–1005

    PubMed  CAS  Google Scholar 

  • Ludlow M, Ennion S (2006) A putative Dictyostelium discoideum P2X receptor. Purinergic Signal 2:81–82

    Google Scholar 

  • Luo J, Yin GF, Gu YZ, Liu Y, Dai JP, Li C, Li ZW (2006) Characterization of three types of ATP-activated current in relation to P2X subunits in rat trigeminal ganglion neurons. Brain Res 1115:9–15

    PubMed  CAS  Google Scholar 

  • Ma W, Quirion R (2007) Inflammatory mediators modulating the transient receptor potential vanilloid 1 receptor: therapeutic targets to treat inflammatory and neuropathic pain. Expert Opin Ther Targets 11:307–320

    PubMed  Google Scholar 

  • Maggi CA, Meli A (1988) The sensory-efferent function of capsaicin-sensitive sensory neurons. Gen Pharmacol 19:1–43

    PubMed  CAS  Google Scholar 

  • Makowska A, Panfil C, Ellrich J (2006) ATP induces sustained facilitation of craniofacial nociception through P2X receptors on neck muscle nociceptors in mice. Cephalalgia 26:697–706

    PubMed  CAS  Google Scholar 

  • Matsuka Y, Neubert JK, Maidment NT, Spigelman I (2001) Concurrent release of ATP and substance P within guinea pig trigeminal ganglia in vivo. Brain Res 915:248–255

    PubMed  CAS  Google Scholar 

  • Matsuka Y, Edmonds B, Mitrirattanakul S, Schweizer FE, Spigelman I (2007) Two types of neurotransmitter release patterns in isolectin B4-positive and negative trigeminal ganglion neurons. Neuroscience 144:665–674

    PubMed  CAS  Google Scholar 

  • Maul E, Sears M (1979) ATP is released into the rabbit eye by antidromic stimulation of the trigeminal nerve. Invest Ophthalmol Vis Sci 18:256–262

    PubMed  CAS  Google Scholar 

  • McGaraughty S, Jarvis MF (2006) Purinergic control of neuropathic pain. Drug Dev Res 67:376–388

    CAS  Google Scholar 

  • McGaraughty S, Chu KL, Namovic MT, Donnelly-Roberts DL, Harris RR, Zhang XF, Shieh CC, Wismer CT, Zhu CZ, Gauvin DM, Fabiyi AC, Honore P, Gregg RJ, Kort ME, Nelson DW, Carroll WA, Marsh K, Faltynek CR, Jarvis MF (2007) P2X7-related modulation of pathological nociception in rats. Neuroscience 146:1817–1828

    PubMed  CAS  Google Scholar 

  • McQueen DS, Bond SM, Moores C, Chessell I, Humphrey PP, Dowd E (1998) Activation of P2X receptors for adenosine triphosphate evokes cardiorespiratory reflexes in anaesthetized rats. J Physiol 507:843–855

    PubMed  CAS  Google Scholar 

  • Millward-Sadler SJ, Wright MO, Flatman PW, Salter DM (2004) ATP in the mechanotransduction pathway of normal human chondrocytes. Biorheology 41:567–575

    PubMed  CAS  Google Scholar 

  • Mishra SK, Braun N, Shukla V, Füllgrabe M, Schomerus C, Korf HW, Gachet C, Ikehara Y, Sévigny J, Robson SC, Zimmermann H (2006) Extracellular nucleotide signaling in adult neural stem cells: synergism with growth factor-mediated cellular proliferation. Development 133:675–684

    PubMed  CAS  Google Scholar 

  • Monro RL, Bertrand PP, Bornstein JC (2004) ATP participates in three excitatory postsynaptic potentials in the submucous plexus of the guinea pig ileum. J Physiol 556:51–584

    Google Scholar 

  • Moore KH, Ray FR, Barden JA (2001) Loss of purinergic P2X3 and P2X5 receptor innervation in human detrusor from adults with urge incontinence. J Neurosci 21:C166:1–6

    Google Scholar 

  • Mori M, Tsushima H Matsuda T (1994) Antidiuretic effects of ATP induced by microinjection into the hypothalamic supraoptic nucleus in water-loaded and ethanol-anesthetized rats. Jpn J Pharmacol 66:445–450

    PubMed  CAS  Google Scholar 

  • Mulkey DK, Mistry AM, Guyenet PG, Bayliss DA (2006) Purinergic P2 receptors modulate excitability but do not mediate pH sensitivity of RTN respiratory chemoreceptors. J Neurosci 26:7230–7233

    PubMed  CAS  Google Scholar 

  • Nagamine K, Ozaki N, Shinoda M, Asai H, Nishiguchi H, Mitsudo K, Tohnai I, Ueda M, Sugiura Y (2006) Mechanical allodynia and thermal hyperalgesia induced by experimental squamous cell carcinoma of the lower gingiva in rats. J Pain 7:659–670

    PubMed  Google Scholar 

  • Nakatsuka T, Gu JG (2006) P2X purinoceptors and sensory transmission. Pflugers Arch Eur J Physiol 452:598–607

    CAS  Google Scholar 

  • Nakatsuka T, Tsuzuki K, Ling JX, Sonobe H, Gu JG (2003) Distinct roles of P2X receptors in modulating glutamate release at different primary sensory synapses in rat spinal cord. J Neurophysiol 89:3243–3252

    PubMed  CAS  Google Scholar 

  • Nazif O, Teichman JM, Gebhart GF (2007) Neural upregulation in interstitial cystitis. Urology 69:24–33

    PubMed  Google Scholar 

  • Neal M, Cunningham J (1994) Modulation by endogenous ATP of the light-evoked release of ACh from retinal cholinergic neurones. Br J Pharmacol 113:1085–1087

    PubMed  CAS  Google Scholar 

  • Nelson DW, Gregg RJ, Kort ME, Perez-Medrano A, Voight EA, Wang Y, Grayson G, Namovic MT, Donnelly-Roberts DL, Niforatos W, Honore P, Jarvis MF, Faltynek CR, Carroll WA (2006) Structure-activity relationship studies on a series of novel, substituted 1-benzyl-5-phenyltetrazole P2X7 antagonists. J Med Chem 49:3659–3666

    PubMed  CAS  Google Scholar 

  • North RA (2002) Molecular physiology of P2X receptors. Physiol Rev 82:1013–1067

    PubMed  CAS  Google Scholar 

  • North RA, Verkhratsky A (2006) Purinergic transmission in the central nervous system. Pflugers Arch Eur J Physiol 452:479–485

    CAS  Google Scholar 

  • Norton WHJ, Rohr KB, Burnstock G (2000) Embryonic expression of a P2X3 receptor encoding gene in zebrafish. Mech Dev 99:149–152

    PubMed  CAS  Google Scholar 

  • Nurse CA (2005) Neurotransmission and neuromodulation in the chemosensory carotid body. Auton Neurosci 120:1–9

    PubMed  CAS  Google Scholar 

  • Okuse K (2007) Pain signalling pathways: from cytokines to ion channels. Int J Biochem Cell Biol 39:490–496

    PubMed  CAS  Google Scholar 

  • Oliveira MC, Parada CA, Veiga MC, Rodrigues LR, Barros SP, Tambeli CH (2005) Evidence for the involvement of endogenous ATP and P2X receptors in TMJ pain. Eur J Pain 9:87–93

    PubMed  CAS  Google Scholar 

  • Pandita RK, Andersson KE (2002) Intravesical adenosine triphosphate stimulates the micturition reflex in awake, freely moving rats. J Urol 168:1230–1234

    PubMed  CAS  Google Scholar 

  • Papka RE, Hafemeister J, Storey-Workley M (2005) P2X receptors in the rat uterine cervix, lumbosacral dorsal root ganglia, and spinal cord during pregnancy. Cell Tissue Res 321:35–44

    PubMed  CAS  Google Scholar 

  • Patel MK, Khakh BS, Henderson G (2001) Properties of native P2X receptors in rat trigeminal mesencephalic nucleus neurones: lack of correlation with known, heterologously expressed P2X receptors. Neuropharmacology 40:96–105

    PubMed  CAS  Google Scholar 

  • Paton JF, De Paula PM, Spyer KM, Machado BH, Boscan P (2002) Sensory afferent selective role of P2 receptors in the nucleus tractus solitarii for mediating the cardiac component of the peripheral chemoreceptor reflex in rats. J Physiol 543:995–1005

    PubMed  CAS  Google Scholar 

  • Pelleg A, Hurt CM (1990) Evidence for ATP-triggered vagal reflex in the canine heart in vivo. Ann N Y Acad Sci 603:441–442

    Google Scholar 

  • Piazza V, Ciubotaru CD, Gale JE, Mammano F (2007) Purinergic signalling and intercellular Ca2+ wave propagation in the organ of Corti. Cell Calcium 41:77–86

    PubMed  CAS  Google Scholar 

  • Pintelon I, Brouns I, De Proost I, Van Meir F, Timmermans JP, Adriaensen D (2007) Sensory receptors in the visceral pleura: neurochemical coding and live staining in whole mounts. Am J Respir Cell Mol Biol 36:541–551

    PubMed  CAS  Google Scholar 

  • Pintor J (2000) Purinergic signalling in the eye. In: Burnstock G, Sillito AM (eds) Nervous control of the eye. Harwood, Amsterdam, pp 171–210

    Google Scholar 

  • Pintor J, Peral A, Pelaez T, Martin S, Hoyle CH (2003) Presence of diadenosine polyphosphates in the aqueous humor: their effect on intraocular pressure. J Pharmacol Exp Therap 304:342–348

    CAS  Google Scholar 

  • Poelchen W, Sieler D, Wirkner K, Illes P (2001) Co-transmitter function of ATP in central catecholaminergic neurons of the rat. Neuroscience 102:593–602

    PubMed  CAS  Google Scholar 

  • Puthussery T, Fletcher EL (2006) P2X2 receptors on ganglion and amacrine cells in cone pathways of the rat retina. J Comp Neurol 496:595–609

    PubMed  CAS  Google Scholar 

  • Puthussery T, Fletcher EL (2007) Neuronal expression of P2X3 purinoceptors in the rat retina. Neuroscience 146:403–414

    PubMed  CAS  Google Scholar 

  • Puthussery T, Yee P, Vingrys AJ, Fletcher EL (2006) Evidence for the involvement of purinergic P2X7 receptors in outer retinal processing. Eur J Neurosci 24:7–19

    PubMed  Google Scholar 

  • Raybould HE, Cooke HJ, Christofi FL (2004) Sensory mechanisms: transmitters, modulators and reflexes. Neurogastroenterol Motil 16:60–63

    PubMed  Google Scholar 

  • Ren Y, Zou X, Fang L, Lin Q (2006) Involvement of peripheral purinoceptors in sympathetic modulation of capsaicin-induced sensitization of primary afferent fibers. J Neurophysiol 96:2207–2216

    PubMed  CAS  Google Scholar 

  • Renton T, Yiangou Y, Baecker PA, Ford AP, Anand P (2003) Capsaicin receptor VR1 and ATP purinoceptor P2X3 in painful and nonpainful human tooth pulp. J Orofac Pain 17:245–250

    PubMed  Google Scholar 

  • Resta V, Novelli E, Vozzi G, Scarpa C, Caleo M, Ahluwalia A, Solini A, Santini E, Parisi V, Di Virgilio F, Galli-Resta L (2007) Acute retinal ganglion cell injury caused by intraocular pressure spikes is mediated by endogenous extracellular ATP. Eur J Neurosci 25:2741–2754

    PubMed  Google Scholar 

  • Reyes EP, Fernández R, Larraín C, Zapata P (2007) Effects of combined cholinergic-purinergic block upon cat carotid body chemoreceptors in vitro. Respir Physiol Neurobiol 156:17–22

    PubMed  CAS  Google Scholar 

  • Rich PB, Douillet CD, Mahler SA, Husain SA, Boucher RC (2003) Adenosine triphosphate is released during injurious mechanical ventilation and contributes to lung edema. J Trauma 55:290–297

    PubMed  CAS  Google Scholar 

  • Robinson DR, McNaughton PA, Evans ML, Hicks GA (2004) Characterization of the primary spinal afferent innervation of the mouse colon using retrograde labelling. Neurogastroenterol Motil 16:113–124

    PubMed  CAS  Google Scholar 

  • Rocha I, Burnstock G, Spyer KM (2001) Effect on urinary bladder function and arterial blood pressure of the activation of putative purine receptors in brainstem areas. Auton Neurosci 88:6–15

    PubMed  CAS  Google Scholar 

  • Romanov RA, Rogachevskaja OA, Bystrova MF, Jiang P, Margolskee RF, Kolesnikov SS (2007) Afferent neurotransmission mediated by hemichannels in mammalian taste cells. EMBO J 26:657–667

    PubMed  CAS  Google Scholar 

  • Rong W, Burnstock G (2004) Activation of ureter nociceptors by exogenous and endogenous ATP in guinea pig. Neuropharmacology 47:1093–1101

    PubMed  CAS  Google Scholar 

  • Rong W, Burnstock G, Spyer KM (2000) P2X purinoceptor-mediated excitation of trigeminal lingual nerve terminals in an in vitro intra-arterially perfused rat tongue preparation. J Physiol 524:891–902

    PubMed  CAS  Google Scholar 

  • Rong W, Gourine A, Cockayne DA, Xiang Z, Ford APDW, Spyer KM, Burnstock G (2003) Pivotal role of nucleotide P2X2 receptor subunit mediating ventilatory responses to hypoxia: knockout mouse studies. J Neurosci 23:11315–11321

    PubMed  CAS  Google Scholar 

  • Ruan H-Z, Burnstock G (2003) Localisation of P2Y1 and P2Y4 receptors in dorsal root, nodose and trigeminal ganglia of the rat. Histochem Cell Biol 120:415–426

    PubMed  CAS  Google Scholar 

  • Ruan H-Z, Moules E, Burnstock G (2004) Changes in P2X purinoceptors in sensory ganglia of the mouse during embryonic and postnatal development. Histochem Cell Biol 122:539–551

    PubMed  CAS  Google Scholar 

  • Ruan H-Z, Birder LA, de Groat WC, Tai C, Roppolo J, Buffington A, Burnstock G (2005) Localization of P2X and P2Y receptors in dorsal root ganglia of the cat. J Histochem Cytochem 53:1273–1282

    PubMed  CAS  Google Scholar 

  • Ruan T, Lin YS, Lin KS, Kou YR (2006) Mediator mechanisms involved in TRPV1 and P2X receptor-mediated, ROS-evoked bradypneic reflex in anesthetized rats. J Appl Physiol 101:644–654

    PubMed  CAS  Google Scholar 

  • Rubino A, Burnstock G (1996) Capsaicin-sensitive sensory-motor neurotransmission in the peripheral control of cardiovascular function. Cardiovasc Res 31:467–479

    PubMed  CAS  Google Scholar 

  • Ruggieri MR Sr (2006) Mechanisms of disease: role of purinergic signaling in the pathophysiology of bladder dysfunction. Nat Clin Pract Urol 3:206–215

    PubMed  CAS  Google Scholar 

  • Salas NA, Somogyi GT, Gangitano DA, Boone TB, Smith CP (2007) Receptor activated bladder and spinal ATP release in neurally intact and chronic spinal cord injured rats. Neurochem Int 50:45–350

    Google Scholar 

  • Salter MW, Henry JL (1985) Effects of adenosine 5′-monophosphate and adenosine 5′-triphosphate on functionally identified units in the cat spinal dorsal horn. Evidence for a differential effect of adenosine 5′-triphosphate on nociceptive vs non-nociceptive units. Neuroscience 15:15–825

    Google Scholar 

  • Schwiebert EM, Zsembery A, Geibel JP (2003) Cellular mechanisms and physiology of nucleotide and nucleoside release from cells: current knowledge, novel assays to detect purinergic agonists, and future directions. Curr Top Membr 54:31–58

    CAS  Google Scholar 

  • Scislo TJ, Ichinose T, O'Leary DS (2007) Activation of NTS A1 adenosine receptors differentially resets baroreflex control of adrenal (ASNA) and renal (RSNA) sympathetic nerve activity. FASEB J 21:582.15

    Google Scholar 

  • Seino D, Tokunaga A, Tachibana T, Yoshiya S, Dai Y, Obata K, Yamanaka H, Kobayashi K, Noguchi K (2006) The role of ERK signaling and the P2X receptor on mechanical pain evoked by movement of inflamed knee joint. Pain 123:193–203

    PubMed  CAS  Google Scholar 

  • Sharp CJ, Reeve AJ, Collins SD, Martindale JC, Summerfield SG, Sargent BS, Bate ST, Chessell IP (2006) Investigation into the role of P2X3/P2X2/3 receptors in neuropathic pain following chronic constriction injury in the rat: an electrophysiological study. Br J Pharmacol 148:845–852

    PubMed  CAS  Google Scholar 

  • Shen J, Harada N, Nakazawa H, Kaneko T, Izumikawa M, Yamashita T (2006) Role of nitric oxide on ATP-induced Ca2+ signaling in outer hair cells of the guinea pig cochlea. Brain Res 1081:101–112

    PubMed  CAS  Google Scholar 

  • Shieh C-C, Jarvis MF, Lee C-H, Perner RJ (2006) P2X receptor ligands and pain. Expert Opin Ther Patents 16:1113–1127

    CAS  Google Scholar 

  • Shimizu I, Iida T, Guan Y, Zhao C, Raja SN, Jarvis MF, Cockayne DA, Caterina MJ (2005) Enhanced thermal avoidance in mice lacking the ATP receptor P2X3. Pain 116:96–108

    PubMed  CAS  Google Scholar 

  • Shinoda M, Ozaki N, Asai H, Nagamine K, Sugiura Y (2005) Changes in P2X3 receptor expression in the trigeminal ganglion following monoarthritis of the temporomandibular joint in rats. Pain 116:42–51

    PubMed  CAS  Google Scholar 

  • Shiokawa H, Nakatsuka T, Furue H, Tsuda M, Katafuchi T, Inoue K, Yoshimura M (2006) Direct excitation of deep dorsal horn neurones in the rat spinal cord by the activation of postsynaptic P2X receptors. J Physiol 573:753–763

    PubMed  CAS  Google Scholar 

  • Smith CP, Vemulakonda VM, Kiss S, Boone TB, Somogyi GT (2005) Enhanced ATP release from rat bladder urothelium during chronic bladder inflammation: effect of botulinum toxin A. Neurochem Int 47:291–297

    PubMed  CAS  Google Scholar 

  • Song Z, Sladek CD (2006) Site of ATP and phenylephrine synergistic stimulation of vasopressin release from the hypothalamo-neurohypophyseal system. J Neuroendocrinol 18:266–272

    PubMed  CAS  Google Scholar 

  • Song Z, Vijayaraghavan S, Sladek CD (2007) ATP increases intracellular calcium in supraoptic neurons by activation of both P2X and P2Y purinergic receptors. Am J Physiol Regul Integr Comp Physiol 292:R423–R431

    PubMed  CAS  Google Scholar 

  • Sorimachi M, Wakamoria M, Akaikeb N (2006) Excitatory effect of ATP on rat area postrema neurons. Purinergic Signal 2:545–557

    Google Scholar 

  • Spyer KM, Dale N, Gourine AV (2004) ATP is a key mediator of central and peripheral chemosensory transduction. Exp Physiol 89:53–59

    PubMed  CAS  Google Scholar 

  • Staikopoulos V, Sessle BJ, Furness JB, Jennings EA (2007) Localization of P2X2 and P2X3 receptors in rat trigeminal ganglion neurons. Neuroscience 144:208–216

    PubMed  CAS  Google Scholar 

  • Stone LS, Vulchanova L (2003) The pain of antisense: in vivo application of antisense oligonucleotides for functional genomics in pain and analgesia. Adv Drug Deliv Rev 55:1081–1112

    PubMed  CAS  Google Scholar 

  • Stucky CL, Medler KA, Molliver DC (2004) The P2Y agonist UTP activates cutaneous afferent fibers. Pain 109:36–44

    PubMed  CAS  Google Scholar 

  • Szücs A, Szappanos H, Batta TJ, Tóth A, Szigeti GP, Panyi G, Csernoch L, Sziklai I (2006) Changes in purinoceptor distribution and intracellular calcium levels following noise exposure in the outer hair cells of the guinea pig. J Membr Biol 213:135–141

    PubMed  Google Scholar 

  • Taylor-Clark T, Undem BJ (2006) Transduction mechanisms in airway sensory nerves. J Appl Physiol 101:950–959

    PubMed  CAS  Google Scholar 

  • Tempest HV, Dixon AK, Turner WH, Elneil S, Sellers LA, Ferguson DR (2004) P2X and P2X receptor expression in human bladder urothelium and changes in interstitial cystitis. BJU Int 93:1344–1348

    PubMed  CAS  Google Scholar 

  • Terasawa E, Keen KL, Grendell RL, Golos TG (2005) Possible role of 5′-adenosine triphosphate in synchronization of Ca2+ oscillations in primate luteinizing hormone-releasing hormone neurons. Mol Endocrinol 19:2736–2747

    PubMed  CAS  Google Scholar 

  • Trang T, Beggs S, Salter MW (2006) Purinoceptors in microglia and neuropathic pain. Pflugers Arch Eur J Physiol 452:645–652

    CAS  Google Scholar 

  • Trapido-Rosenthal HG, Carr WE, Gleeson RA (1989) Biochemistry of purinergic olfaction. The importance of nucleotide dephosphorylation. In: Brand JG, Teeter H, Cagan RH, Kare MR (eds) Receptor events and transduction in taste and olfaction. Chemical senses, vol 1. Dekker, New York, pp 243–262

    Google Scholar 

  • Tsuda M, Inoue K (2006) P2X receptors in sensory neurons. Curr Top Membr 57:277–310

    CAS  Google Scholar 

  • Tsuda M, Shigemoto-Mogami Y, Koizumi S, Mizokoshi A, Kohsaka S, Salter MW, Inoue K (2003) P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 424:778–783

    PubMed  CAS  Google Scholar 

  • Undem BJ, Chuaychoo B, Lee MG, Weinreich D, Myers AC, Kollarik M (2004) Subtypes of vagal afferent C-fibres in guinea-pig lungs. J Physiol 556:905–917

    PubMed  CAS  Google Scholar 

  • US 2005/0209260 A1 (Hoffmann-La Roche Pharmaceuticals) Broka CA, Carter DS, Dillon MP, Hawley RC, Jahangir A, Lin CJJ, Parish DW (Sep 22, 2005). Diaminopyrimidines as P2X3 and P2X2/3 antagonists.

    Google Scholar 

  • Vlajkovic SM, Vinayagamoorthy A, Thorne PR, Robson SC, Wang CJ, Housley GD (2006) Noise-induced up-regulation of NTPDase3 expression in the rat cochlea: implications for auditory transmission and cochlear protection. Brain Res 1104:55–63

    PubMed  CAS  Google Scholar 

  • Vlaskovska M, Kasakov L, Rong W, Bodin P, Bardini M, Cockayne DA, Ford APDW, Burnstock G (2001) P2X3 knockout mice reveal a major sensory role for urothelially released ATP. J Neurosci 21:5670–5677

    PubMed  CAS  Google Scholar 

  • Waeber C, Moskowitz MA (2003) Therapeutic implications of central and peripheral neurologic mechanisms in migraine. Neurology 61:S9–S20

    PubMed  Google Scholar 

  • Wang JC, Raybould NP, Luo L, Ryan AF, Cannell MB, Thorne PR, Housley GD (2003) Noise induces up-regulation of P2X2 receptor subunit of ATP-gated ion channels in the rat cochlea. Neuroreport 14:817–823

    PubMed  CAS  Google Scholar 

  • Wang LC, Xiong W, Zheng J, Zhou Y, Zheng H, Zhang C, Zheng LH, Zhu XL, Xiong ZQ, Wang LY, Cheng HP, Zhou Z (2006) The timing of endocytosis after activation of a G-protein-coupled receptor in a sensory neuron. Biophys J 90:3590–3598

    PubMed  CAS  Google Scholar 

  • Watano T, Calvert JA, Vial C, Forsythe ID, Evans RJ (2004) P2X receptor subtype-specific modulation of excitatory and inhibitory synaptic inputs in the rat brainstem. J Physiol 558:745–757

    PubMed  CAS  Google Scholar 

  • Werner-Reiss U, Galun R, Crnjar R, Liscia A (1999) Sensitivity of the mosquito Aedes aegypti (Culicidae) labral apical chemoreceptors to phagostimulants. J Insect Physiol 45:629–636

    PubMed  CAS  Google Scholar 

  • Wheeler-Schilling TH, Marquordt K, Kohler K, Guenther E, Jabs R (2001) Identification of purinergic receptors in retinal ganglion cells. Brain Res Mol Brain Res 92:177–180

    PubMed  CAS  Google Scholar 

  • Wong AY, Billups B, Johnston J, Evans RJ, Forsythe ID (2006) Endogenous activation of adenosine A1 receptors, but not P2X receptors, during high-frequency synaptic transmission at the calyx of Held. J Neurophysiol 95:3336–3342

    PubMed  CAS  Google Scholar 

  • Wu C, Sui GP, Fry CH (2004) Purinergic regulation of guinea pig suburothelial myofibroblasts. J Physiol 559:231–243

    PubMed  CAS  Google Scholar 

  • Wynn G, Rong W, Xiang Z, Burnstock G (2003) Purinergic mechanisms contribute to mechanosensory transduction in the rat colorectum. Gastroenterology 125:1398–1409

    PubMed  CAS  Google Scholar 

  • Wynn G, Bei M, Ruan H-Z, Burnstock G (2004) Purinergic component of mechanosensory transduction is increased in a rat model of colitis. Am J Physiol Gastrointest Liver Physiol 287:G647–G657

    PubMed  CAS  Google Scholar 

  • Xiang Z, Burnstock G (2004a) P2X2 and P2X3 purinoceptors in the rat enteric nervous system. Histochem Cell Biol 121:169–179

    PubMed  CAS  Google Scholar 

  • Xiang Z, Burnstock G (2004b) Development of nerves expressing P2X3 receptors in the myenteric plexus of rat stomach. Histochem Cell Biol 122:111–119

    PubMed  CAS  Google Scholar 

  • Xiang Z, Burnstock G (2006) Distribution of P2Y6 and P2Y12 receptors: their colocalisation with calbindin, calretinin and nitric oxide synthase in the guinea pig enteric nervous system. Histochem Cell Biol 125:327–336

    PubMed  CAS  Google Scholar 

  • Xiang Z, He C, Burnstock G (2006) P2X5 receptors are expressed on neurons containing arginine vasopressin and neuronal nitric oxide synthase in the rat hypothalamus. Brain Res 1099:56–63

    PubMed  CAS  Google Scholar 

  • Xu J, Kussmaul W, Kurnik PB, Al-Ahdav M, Pelleg A (2005) Electrophysiological-anatomic correlates of ATP-triggered vagal reflex in the dog. V. Role of purinergic receptors. Am J Physiol Regul Integr Comp Physiol 288:R651–R655

    PubMed  CAS  Google Scholar 

  • Xue J, Askwith C, Javed NH, Cooke HJ (2007) Autonomic nervous system and secretion across the intestinal mucosal surface. Auton Neurosci 133:55–63

    PubMed  CAS  Google Scholar 

  • Yajima H, Sato J, Giron R, Nakamura R, Mizumura K (2005) Inhibitory, facilitatory, and excitatory effects of ATP and purinergic receptor agonists on the activity of rat cutaneous nociceptors in vitro. Neurosci Res 51:405–416

    PubMed  CAS  Google Scholar 

  • Yu S, Undem BJ, Kollarik M (2005) Vagal afferent nerves with nociceptive properties in guinea-pig oesophagus. J Physiol 563:831–842

    PubMed  CAS  Google Scholar 

  • Zagorodnyuk VP, Chen BN, Costa M, Brookes SJ (2003) Mechanotransduction by intraganglionic laminar endings of vagal tension receptors in the guinea-pig oesophagus. J Physiol 553:575–587

    PubMed  CAS  Google Scholar 

  • Zapata P (2007) Is ATP a suitable co-transmitter in carotid body arterial chemoreceptors? Respir Physiol Neurobiol 157:106–115

    PubMed  CAS  Google Scholar 

  • Zarei MM, Toro B, McCleskey EW (2004) Purinergic synapses formed between rat sensory neurons in primary culture. Neuroscience 126:195–201

    PubMed  CAS  Google Scholar 

  • Zhang M, Nurse CA (2004) CO2/pH chemosensory signaling in co-cultures of rat carotid body receptors and petrosal neurons: role of ATP and ACh. J Neurophysiol 92:3433–3445

    PubMed  CAS  Google Scholar 

  • Zhang X, Zhang M, Laties AM, Mitchell CH (2005) Stimulation of P2X7 receptors elevates Ca2+ and kills retinal ganglion cells. Invest Ophthalmol Vis Sci 46:2183–2191

    PubMed  Google Scholar 

  • Zhang X, Zhang M, Laties AM, Mitchell CH (2006) Balance of purines may determine life or death of retinal ganglion cells as A3 adenosine receptors prevent loss following P2X7 receptor stimulation. J Neurochem 98:566–575

    PubMed  CAS  Google Scholar 

  • Zhang M, Buttigieg J, Nurse CA (2007a) Neurotransmitter mechanisms mediating low-glucose signalling in cocultures and fresh tissue slices of rat carotid body. J Physiol 578:735–750

    PubMed  CAS  Google Scholar 

  • Zhang X, Chen Y, Wang C, Huang LY (2007b) Neuronal somatic ATP release triggers neuron-satellite glial cell communication in dorsal root ganglia. Proc Natl Acad Sci USA 104:9864–9869

    PubMed  CAS  Google Scholar 

  • Zimmermann H (2006) Nucleotide signaling in nervous system development. Pflugers Arch Eur J Physiol 452:573–588

    CAS  Google Scholar 

  • Zimmermann K, Reeh PW, Averbeck B (2002) ATP can enhance the proton-induced CGRP release through P2Y receptors and secondary PGE2 release in isolated rat dura mater. Pain 97:259–265

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Geoffrey Burnstock .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Burnstock, G. (2009). Purines and Sensory Nerves. In: Canning, B., Spina, D. (eds) Sensory Nerves. Handbook of Experimental Pharmacology, vol 194. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-79090-7_10

Download citation

Publish with us

Policies and ethics