The Journal of Pain
Volume 11, Issue 3 , Pages 210-218 , March 2010

ASIC1 and ASIC3 Play Different Roles in the Development of Hyperalgesia After Inflammatory Muscle Injury

  • Roxanne Y. Walder

      Affiliations

    • Physical Therapy and Rehabilitation Science, Pain Research Program, University of Iowa, Iowa City, Iowa
    • ,
  • Lynn A. Rasmussen

      Affiliations

    • Physical Therapy and Rehabilitation Science, Pain Research Program, University of Iowa, Iowa City, Iowa
    • ,
  • Jon D. Rainier

      Affiliations

    • Department of Chemistry, University of Utah, Salt Lake City, Utah
    • ,
  • Alan R. Light

      Affiliations

    • Department of Anesthesiology, University of Utah, Salt Lake City, Utah
    • ,
  • John A. Wemmie

      Affiliations

    • Department of Psychiatry, University of Iowa, Iowa City, Iowa
    • Department of Veterans Affairs Medical Center, Iowa City, Iowa
    • ,
  • Kathleen A. Sluka

      Affiliations

    • Physical Therapy and Rehabilitation Science, Pain Research Program, University of Iowa, Iowa City, Iowa
    • Corresponding Author InformationAddress reprint requests to Dr Kathleen A. Sluka, Graduate Program in Physical Therapy and Rehabilitation Science, 1-242 MEB, University of Iowa, Iowa City, IA 52242.

Received 18 May 2009 ,Revised 1 July 2009 ,Accepted 13 July 2009.

References 

  1. Akopian AN, Chen CC, Ding Y, Cesare P, Wood JN. A new member of the acid-sensing ion channel family. Neuroreport. 2000;11:2217–2222
  2. Allen NJ, Attwell D. Modulation of ASIC channels in rat cerebellar Purkinje neurons by ischaemia-related signals. J Physiol. 2002;543:521–529
  3. Alvarez de la Rosa D, Krueger SR, Kolar A, Shao D, Fitzsimonds RM, Canessa CM. Distribution, subcellular localization and ontogeny of ASIC1 in the mammalian central nervous system. J Physiol. 2003;546:77–87
  4. Askwith CC, Cheng C, Ikuma M, Benson C, Price MP, Welsh MJ. Neuropeptide FF and FMRFamide potentiate acid-evoked currents from sensory neurons and proton-gated DEG/ENaC channels. Neuron. 2000;26:133–141
  5. Askwith CC, Wemmie JA, Price MP, Rokhlina T, Welsh MJ. Acid-sensing ion channel 2 (ASIC2) modulates ASIC1 H+-activated currents in hippocampal neurons. J Biol Chem. 2004;279:18296–18305
  6. Babinski K, Le KT, Seguela P. Molecular cloning and regional distribution of a human proton receptor subunit with biphasic functional properties. J Neurochem. 1999;72:51–57
  7. Babinski K, Catarsi S, Biagini G, Seguela P. Mammalian ASIC2a and ASIC3 subunits co-assemble into heteromeric proton-gated channels sensitive to Gd3+. J Biol Chem. 2000;275:28519–28525
  8. Baron A, Waldmann R, Lazdunski M. ASIC-like, proton-activated currents in rat hippocampal neurons. J Physiol. 2002;539:485–494
  9. Baron A, Voilley N, Lazdunski M, Lingueglia E. Acid sensing ion channels in dorsal spinal cord neurons. J Neurosci. 2008;28:1498–1508
  10. Bassilana F, Champigny G, Waldmann R, de Weille JR, Heurteaux C, Lazdunski M. The acid-sensitive ionic channel subunit ASIC and the mammalian degenerin MDEG form a heteromultimeric H+-gated Na+ channel with novel properties. J Biol Chem. 1997;272:28819–28822
  11. Benson CJ, Xie J, Wemmie JA, Price MP, Henss JM, Welsh MJ, et al. Heteromultimers of DEG/ENaC subunits form H+-gated channels in mouse sensory neurons. Proc Natl Acad Sci USA. 2002;99:2338–2343
  12. Bileviciute I, Stenfors C, Theodorsson E, Lundeberg T. Unilateral injection of calcitonin gene-related peptide (CGRP) induces bilateral oedema formation and release of CGRP-like immunoreactivity in the rat hindpaw. Br J Pharmacol. 1998;125:1304–1312
  13. Carnally SM, Dev HS, Stewart AP, Barrera NP, Van Bemmelen MX, Schild L, et al. Direct visualization of the trimeric structure of the ASIC1a channel, using AFM imaging. Biochem Biophys Res Commun. 2008;372:752–755
  14. Catarsi S, Babinski K, Seguela P. Selective modulation of heteromeric ASIC proton-gated channels by neuropeptide FF. Neuropharmacology. 2001;41:592–600
  15. Chen CC, England S, Akopian AN, Wood JN. A sensory neuron-specific, proton-gated ion channel. Proc Natl Acad Sci USA. 1998;95:10240–10245
  16. Chen CC, Zimmer A, Sun WH, Hall J, Brownstein MJ, Zimmer A. A role for ASIC3 in the modulation of high-intensity pain stimuli. Proc Natl Acad Sci USA. 2002;99:8992–8997
  17. Chen X, Kalbacher H, Grunder S. The tarantula toxin psalmotoxin 1 inhibits acid-sensing ion channel (ASIC) 1a by increasing its apparent H+ affinity. J Gen Physiol. 2005;126:71–79
  18. Chen X, Kalbacher H, Grunder S. Interaction of acid-sensing ion channel (ASIC) 1 with the tarantula toxin psalmotoxin 1 is state dependent. J Gen Physiol. 2006;127:267–276
  19. Coryell MW, Ziemann AE, Westmoreland PJ, Haenfler JM, Kurjakovic Z, Zha XM, et al. Targeting ASIC1a reduces innate fear and alters neuronal activity in the fear circuit. Biol Psychiatry. 2007;62:1140–1148
  20. Coscoy S, Lingueglia E, Lazdunski M, Barbry P. The Phe-Met-Arg-Phe-amide-activated sodium channel is a tetramer. J Biol Chem. 1998;273:8317–8322
  21. Deval E, Noel J, Lay N, Alloui A, Diochot S, Friend V, et al. ASIC3, a sensor of acidic and primary inflammatory pain. EMBO J. 2008;27:3047–3055
  22. Drew LJ, Rohrer DK, Price MP, Blaver KE, Cockayne DA, Cesare P, et al. Acid-sensing ion channels ASIC2 and ASIC3 do not contribute to mechanically activated currents in mammalian sensory neurones. J Physiol. 2004;556:691–710
  23. Duan B, Wu LJ, Yu YQ, Ding Y, Jing L, Xu L, et al. Upregulation of acid-sensing ion channel ASIC1a in spinal dorsal horn neurons contributes to inflammatory pain hypersensitivity. J Neurosci. 2007;27:11139–11148
  24. Dube GR, Lehto SG, Breese NM, Baker SJ, Wang X, Matulenko MA, et al. Electrophysiological and in vivo characterization of A-317567, a novel blocker of acid sensing ion channels. Pain. 2005;117:88–96
  25. Ferreira J, Santos AR, Calixto JB. Antinociception produced by systemic, spinal and supraspinal administration of amiloride in mice. Life Sci. 1999;65:1059–1066
  26. Garcia-Anoveros J, Derfler B, Neville-Golden J, Hyman BT, Corey DP. BNaC1 and BNaC2 constitute a new family of human neuronal sodium channels related to degenerins and epithelial sodium channels. Proc Natl Acad Sci USA. 1997;94:1459–1464
  27. Grunder S, Geissler HS, Bassler EL, Ruppersberg JP. A new member of acid-sensing ion channels from pituitary gland. Neuroreport. 2000;11:1607–1611
  28. Häbler C. Untersuchungen zur Molekularpathologie der Gelenkexsudate und ihre klinischen Ergebnisse. Arch Klin Chir. 1929;156:20–42
  29. Hesselager M, Timmermann DB, Ahring PK. pH Dependency and desensitization kinetics of heterologously expressed combinations of acid-sensing ion channel subunits. J Biol Chem. 2004;279:11006–11015
  30. Ikeuchi M, Kolker SJ, Burnes LA, Walder RY, Sluka KA. Role of ASIC3 in the primary and secondary hyperalgesia produced by joint inflammation in mice. Pain. 2008;137:662–669
  31. Immke DC, McCleskey EW. ASIC3: A lactic acid sensor for cardiac pain. Sci World J. 2001;1:510–512
  32. Ishibashi K, Marumo F. Molecular cloning of a DEG/ENaC sodium channel cDNA from human testis. Biochem Biophys Res Commun. 1998;245:589–593
  33. Jahr H, van Driel M, van Osch GJ, Weinans H, van Leeuwen JP. Identification of acid-sensing ion channels in bone. Biochem Biophys Res Commun. 2005;337:349–354
  34. Jasti J, Furukawa H, Gonzales EB, Gouaux E. Structure of acid-sensing ion channel 1 at 1.9 A resolution and low pH. Nature. 2007;449:316–323
  35. Jensen K, Tuxen C, Pedersen-Bjergaard U, Jansen I. Pain, tenderness, wheal and flare induced by substance-P, bradykinin and 5-hydroxytryptamine in humans. Cephalalgia. 1991;11:175–182
  36. Kelly S, Dunham JP, Donaldson LF. Sensory nerves have altered function contralateral to a monoarthritis and may contribute to the symmetrical spread of inflammation. Eur J Neurosci. 2007;26:935–942
  37. Krishtal O. The ASICs: Signaling molecules? Modulators?. Trends Neurosci. 2003;26:477–483
  38. Leonard AS, Yermolaieva O, Hruska-Hageman A, Askwith CC, Price MP, Wemmie JA, et al. cAMP-dependent protein kinase phosphorylation of the acid-sensing ion channel-1 regulates its binding to the protein interacting with C-kinase-1. Proc Natl Acad Sci USA. 2003;100:2029–2034
  39. Light AR, Hughen RW, Zhang J, Rainier J, Liu Z, Lee J. Dorsal root ganglion neurons innervating skeletal muscle respond to physiological combinations of protons, ATP, and lactate mediated by ASIC, P2X, and TRPV1. J Neurophysiol. 2008;100:1184–1201
  40. Lingueglia E, de Weille JR, Bassilana F, Heurteaux C, Sakai H, Waldmann R, et al. A modulatory subunit of acid sensing ion channels in brain and dorsal root ganglion cells. J Biol Chem. 1997;272:29778–29783
  41. Lingueglia E. Acid-sensing ion channels in sensory perception. J Biol Chem. 2007;282:17325–17329
  42. Mamet J, Baron A, Lazdunski M, Voilley N. Proinflammatory mediators, stimulators of sensory neuron excitability via the expression of acid-sensing ion channels. J Neurosci. 2002;22:10662–10670
  43. Mamet J, Lazdunski M, Voilley N. How nerve growth factor drives physiological and inflammatory expressions of acid-sensing ion channel 3 in sensory neurons. J Biol Chem. 2003;278:48907–48913
  44. Mazzuca M, Heurteaux C, Alloui A, Diochot S, Baron A, Voilley N, et al. A tarantula peptide against pain via ASIC1a channels and opioid mechanisms. Nat Neurosci. 2007;10:943–945
  45. Mogil JS, Breese NM, Witty MF, Ritchie J, Rainville ML, Ase A, et al. Transgenic expression of a dominant-negative ASIC3 subunit leads to increased sensitivity to mechanical and inflammatory stimuli. J Neurosci. 2005;25:9893–9901
  46. Molliver DC, Immke DC, Fierro L, Pare M, Rice FL, McCleskey EW. ASIC3, an acid-sensing ion channel, is expressed in metaboreceptive sensory neurons. Mol Pain. 2005;1:35
  47. O'Brien C, Woolf CJ, Fitzgerald M, Lindsay RM, Molander C. Differences in the chemical expression of rat primary afferent neurons which innervate skin, muscle or joint. Neuroscience. 1989;32:493–502
  48. Ohtori S, Inoue G, Koshi T, Ito T, Doya H, Saito T, et al. Up-regulation of acid-sensing ion channel 3 in dorsal root ganglion neurons following application of nucleus pulposus on nerve root in rats. Spine. 2006;31:2048–2052
  49. Page AJ, Brierley SM, Martin CM, Price MP, Symonds E, Butler R, et al. Different contributions of ASIC channels 1a, 2, and 3 in gastrointestinal mechanosensory function. Gut. 2005;54:1408–1415
  50. Page AJ, Brierley SM, Martin CM, Hughes PA, Blackshaw LA. Acid sensing ion channels 2 and 3 are required for inhibition of visceral nociceptors by benzamil. Pain. 2007;133:150–160
  51. Pedersen-Bjergaard U, Nielsen LB, Jensen K, Edvinsson L, Jansen I, Olesen J. Calcitonin gene-related peptide, neurokinin A and substance P: Effects on nociception and neurogenic inflammation in human skin and temporal muscle. Peptides. 1991;12:333–337
  52. Plenderleith MB, Snow PJ. The plant lectin Bandeiraea simplicifolia I-B4 identifies a subpopulation of small diameter primary sensory neurones which innervate the skin in the rat. Neurosci Lett. 1993;159:17–20
  53. Poirot O, Berta T, Decosterd I, Kellenberger S. Distinct ASIC currents are expressed in rat putative nociceptors and are modulated by nerve injury. J Physiol. 2006;576:215–234
  54. Price MP, Snyder PM, Welsh MJ. Cloning and expression of a novel human brain Na+ channel. J Biol Chem. 1996;271:7879–7882
  55. Price MP, Lewin GR, McIlwrath SL, Cheng C, Xie J, Heppenstall PA, et al. The mammalian sodium channel BNC1 is required for normal touch sensation. Nature. 2000;407:1007–1011
  56. Price MP, McIlwrath SL, Xie J, Cheng C, Qiao J, Tarr DE, et al. The DRASIC cation channel contributes to the detection of cutaneous touch and acid stimuli in mice. Neuron. 2001;32:1071–1083
  57. Rees H, Sluka KA, Westlund KN, Willis WD. The role of glutamate and GABA receptors in the generation of dorsal root reflexes by acute arthritis in the anaesthetized rat. J Physiol. 1995;484(Pt 2):437–445
  58. Rees H, Sluka KA, Lu Y, Westlund KN, Willis WD. Dorsal root reflexes in articular afferents occur bilaterally in a chronic model of arthritis in rats. J Neurophysiol. 1996;76:4190–4193
  59. Roza C, Puel JL, Kress M, Baron A, Diochot S, Lazdunski M, et al. Knockout of the ASIC2 channel in mice does not impair cutaneous mechanosensation, visceral mechanonociception and hearing. J Physiol. 2004;558:659–669
  60. Salinas M, Rash LD, Baron A, Lambeau G, Escoubas P, Lazdunski M. The receptor site of the spider toxin PcTx1 on the proton-gated cation channel ASIC1a. J Physiol. 2006;570:339–354
  61. Skyba DA, Radhakrishnan R, Sluka KA. Characterization of a method for measuring primary hyperalgesia of deep somatic tissue. J Pain. 2005;6:41–47
  62. Sluka KA, Radhakrishnan R, Price MP, Welsh MJ. ASIC3 mediates mechanical hyperalgesia induced by muscle injury. In:  Brune K,  Handwerker HO editor. Hyperalgesia: Molecular Mechanisms and Clinical Implications. Seattle, WA: IASP Press; 2004;p. 105–112
  63. Sluka KA, Westlund KN. Behavioral and immunohistochemical changes in an experimental arthritis model in rats. Pain. 1993;55:367–377
  64. Sluka KA, Rees H, Westlund KN, Willis WD. Fiber types contributing to dorsal root reflexes induced by joint inflammation in cats and monkeys. J Neurophysiol. 1995;74:981–989
  65. Sluka KA, Price MP, Breese NM, Stucky CL, Wemmie JA, Welsh MJ. Chronic hyperalgesia induced by repeated acid injections in muscle is abolished by the loss of ASIC3, but not ASIC1. Pain. 2003;106:229–239
  66. Sluka KA, Radhakrishnan R, Benson CJ, Eshcol JO, Price MP, Babinski K, et al. ASIC3 in muscle mediates mechanical, but not heat, hyperalgesia associated with muscle inflammation. Pain. 2007;129:102–112
  67. Sluka KA, Westlund-High KN. Neurologic regulation of inflammation. In:  Firestein GS,  Budd RC,  Harris ED,  McInnes IB,  Ruddy S,  Sergent JS editor. Kelley's Textbook of Rheumatology. 8th edition. Philadelphia, PA: Saunders/Elsevier; 2009;p. 411–419
  68. Staniland AA, McMahon SB. Mice lacking acid-sensing ion channels (ASIC) 1 or 2, but not ASIC3, show increased pain behaviour in the formalin test. Eur J Pain. 2009;13:554–563
  69. Ugawa S, Ueda T, Takahashi E, Hirabayashi Y, Yoneda T, Komai S, et al. Cloning and functional expression of ASIC-beta2, a splice variant of ASIC-beta. Neuroreport. 2001;12:2865–2869
  70. Ugawa S, Ueda T, Ishida Y, Nishigaki M, Shibata Y, Shimada S. Amiloride-blockable acid-sensing ion channels are leading acid sensors expressed in human nociceptors. J Clin Invest. 2002;110:1185–1190
  71. Voilley N, de Weille J, Mamet J, Lazdunski M. Nonsteroid anti-inflammatory drugs inhibit both the activity and the inflammation-induced expression of acid-sensing ion channels in nociceptors. J Neurosci. 2001;21:8026–8033
  72. Voilley N. Acid-sensing ion channels (ASICs): New targets for the analgesic effects of non-steroid anti-inflammatory drugs (NSAIDs). Curr Drug Targets Inflamm Allergy. 2004;3:71–79
  73. Waldmann R, Champigny G, Voilley N, Lauritzen I, Lazdunski M. The mammalian degenerin MDEG, an amiloride-sensitive cation channel activated by mutations causing neurodegeneration in Caenorhabditis elegans. J Biol Chem. 1996;271:10433–10436
  74. Waldmann R, Bassilana F, de Weille J, Champigny G, Heurteaux C, Lazdunski M. Molecular cloning of a non-inactivating proton-gated Na+ channel specific for sensory neurons. J Biol Chem. 1997;272:20975–20978
  75. Wall PD, Woolf CJ. Muscle but not cutaneous C-afferent input produces prolonged increases in the excitability of the flexion reflex in the rat. J Physiol. 1984;356:443–458
  76. Wemmie JA, Chen J, Askwith CC, Hruska-Hageman AM, Price MP, Nolan BC, et al. The acid-activated ion channel ASIC contributes to synaptic plasticity, learning, and memory. Neuron. 2002;34:463–477
  77. Wemmie JA, Askwith CC, Lamani E, Cassell MD, Freeman JH, Welsh MJ. Acid-sensing ion channel 1 is localized in brain regions with high synaptic density and contributes to fear conditioning. J Neurosci. 2003;23:5496–5502
  78. Wemmie JA, Price MP, Welsh MJ. Acid-sensing ion channels: Advances, questions and therapeutic opportunities. Trends Neurosci. 2006;29:578–586
  79. Woolf CJ, Wall PD. Relative effectiveness of C primary afferent fibers of different origins in evoking a prolonged facilitation of the flexor reflex in the rat. J Neurosci. 1986;6:1433–1442
  80. Wu LJ, Duan B, Mei YD, Gao J, Chen JG, Zhuo M, et al. Characterization of acid-sensing ion channels in dorsal horn neurons of rat spinal cord. J Biol Chem. 2004;279:43716–43724
  81. Yen YT, Tu PH, Chen CJ, Lin YW, Hsieh ST, Chen CC. Role of acid-sensing ion channel 3 in sub-acute-phase inflammation. Mol Pain. 2009;5:1

PII: S1526-5900(09)00637-3

doi: 10.1016/j.jpain.2009.07.004

The Journal of Pain
Volume 11, Issue 3 , Pages 210-218 , March 2010

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