Sensing muscle ischemia: Coincident detection of acid and ATP via interplay of two ion channels

Neuron

Volumn 68, Issue 4, 2010, Pages 739-749

  Birdsong, William T ^a   Fierro, Leonardo ^a   Williams, Frank G ^b   Spelta, Valeria ^a   Naves, Ligia A ^a   Knowles, Michelle ^a   Marsh Haffner, Josephine ^a   Adelman, John P ^a   Almers, Wolfhard ^a   Elde, Robert P ^b   McCleskey, Edwin W ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACID SENSING ION CHANNEL; ACID SENSING ION CHANNEL 3; ADENOSINE TRIPHOSPHATE; LACTIC ACID; PURINERGIC P2X2 RECEPTOR; PURINERGIC P2X4 RECEPTOR; PURINERGIC P2X5 RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CALCIUM CELL LEVEL; CELLULAR DISTRIBUTION; CHANNEL GATING; CONTROLLED STUDY; EXTRACELLULAR CALCIUM; HUMAN; HUMAN CELL; LACTIC ACIDOSIS; MUSCLE ISCHEMIA; MUSCULOSKELETAL PAIN; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN ASSEMBLY; RAT; SENSORY NERVE CELL; SIGNAL TRANSDUCTION;

ACIDOSIS, LACTIC; ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; ANIMALS; CERCOPITHECUS AETHIOPS; CHO CELLS; COS CELLS; CRICETINAE; CRICETULUS; HEK293 CELLS; HUMANS; HYDROGEN-ION CONCENTRATION; ISCHEMIA; MOLECULAR SEQUENCE DATA; MUSCLE, SKELETAL; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, PURINERGIC P2X5; SENSORY RECEPTOR CELLS; SODIUM CHANNELS;

EID: 78449300659     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2010.09.029     Document Type: Article

References (74)

1. Alam M., Smirk F.H. Observations in man upon a blood pressure raising reflex arising from the voluntary muscles. J. Physiol. 1937, 89:372-383.
2. Babini E., Paukert M., Geisler H.S., Grunder S. Alternative splicing and interaction with di- and polyvalent cations control the dynamic range of acid-sensing ion channel 1 (ASIC1). J. Biol. Chem. 2002, 277:41597-41603.
3. Bautista D.M., Jordt S.E., Nikai T., Tsuruda P.R., Read A.J., Poblete J., Yamoah E.N., Basbaum A.I., Julius D. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 2006, 124:1269-1282.
4. Benson C.J., McCleskey E.W. ASICs function as lactic acid sensors during cardiac ischemia. Molecular Sensors for Cardiovascular Homeostasis 2007, 32-50. Springer, New York. D.H. Wang (Ed.).
5. Benson C.J., Eckert S.P., McCleskey E.W. Acid-evoked currents in cardiac sensory neurons: a possible mediator of myocardial ischemic sensation. Circ. Res. 1999, 84:921-928.
6. Birdsong, W.T. (2008) Acid sensing ion channels: coincident detection of ischemia by a channel-channel interaction. PhD thesis, Oregon Health & Sciences University, Portland, Oregon.
7. Borst M.M., Schrader J. Adenine nucleotide release from isolated perfused guinea pig hearts and extracellular formation of adenosine. Circ. Res. 1991, 68:797-806.
8. Boue-Grabot E., Barajas-Lopez C., Chakfe Y., Blais D., Belanger D., Emerit M.B., Seguela P. Intracellular cross talk and physical interaction between two classes of neurotransmitter-gated channels. J. Neurosci. 2003, 23:1246-1253.
9. Boue-Grabot E., Emerit M.B., Toulme E., Seguela P., Garret M. Cross-talk and co-trafficking between rho1/GABA receptors and ATP-gated channels. J. Biol. Chem. 2004, 279:6967-6975.
10. Bray D., Duke T. Conformational spread: the propagation of allosteric states in large multiprotein complexes. Annu. Rev. Biophys. Biomol. Struct. 2004, 33:53-73.
11. Burnstock G. Physiology and pathophysiology of purinergic neurotransmission. Physiol. Rev. 2007, 87:659-797.
12. Chaumont S., Khakh B.S. Patch-clamp coordinated spectroscopy shows P2X2 receptor permeability dynamics require cytosolic domain rearrangements but not Panx-1 channels. Proc. Natl. Acad. Sci. USA 2008, 105:12063-12068.
13. Ciruela F. Fluorescence-based methods in the study of protein-protein interactions in living cells. Curr. Opin. Biotechnol. 2008, 19:338-343.
14. Cobbe S.M., Poole-Wilson P.A. The time of onset and severity of acidosis in myocardial ischaemia. J. Mol. Cell. Cardiol. 1980, 12:745-760.
15. Collo G., North R.A., Kawashima E., Merlo-Pich E., Neidhart S., Surprenant A., Buell G. Cloning of P2X5 and P2X6 receptors and the distribution and properties of an extended family of ATP-gated ion channels. J. Neurosci. 1996, 16:2495-2507.
16. Cook S.P., Vulchanova L., Hargreaves K.M., Elde R., McCleskey E.W. Distinct ATP receptors on pain-sensing and stretch-sensing neurons. Nature 1997, 387:505-508.
17. Craig A.D. How do you feel? Interoception: the sense of the physiological condition of the body. Nat. Rev. Neurosci. 2002, 3:655-666.
18. Deval E., Noel J., Lay N., Alloui A., Diochot S., Friend V., Jodar M., Lazdunski M., Lingueglia E. ASIC3, a sensor of acidic and primary inflammatory pain. EMBO J. 2008, 27:3047-3055.
19. Eckert S.P., Taddese A., McCleskey E.W. Isolation and culture of rat sensory neurons having distinct sensory modalities. J. Neurosci. Methods 1997, 77:183-190.
20. Fabbretti E., Sokolova E., Masten L., D'Arco M., Fabbro A., Nistri A., Giniatullin R. Identification of negative residues in the P2X3 ATP receptor ectodomain as structural determinants for desensitization and the Ca2+-sensing modulatory sites. J. Biol. Chem. 2004, 279:53109-53115.
21. Forrester T. An estimate of adenosine triphosphate release into the venous effluent from exercising human forearm muscle. J. Physiol. 1972, 224:611-628.
22. Fu L.W., Longhurst J.C. Regulation of cardiac afferent excitability in ischemia. Handb. Exp. Pharmacol. 2009, 194:185-225.
23. Hayashi T., Umemori H., Mishina M., Yamamoto T. The AMPA receptor interacts with and signals through the protein tyrosine kinase Lyn. Nature 1999, 397:72-76.
24. Hayes S.G., McCord J.L., Kaufman M.P. Role played by P2X and P2Y receptors in evoking the muscle chemoreflex. J. Appl. Physiol. 2008, 104:538-541.
25. Hellsten Y., Maclean D., Radegran G., Saltin B., Bangsbo J. Adenosine Concentrations in the Interstitium of Resting and Contracting Human Skeletal Muscle. Circulation 1998, 98:6-8.
26. Hille B. Ion Channels of Excitable Membranes 2001, Sinauer Associates, Inc., Sunderland, MA. Third Edition.
27. Holzer P. Acid-sensitive ion channels and receptors. Handb. Exp. Pharmacol. 2009, 194:283-332.
28. Honig M.G., Hume R.I. Fluorescent carbocyanine dyes allow living neurons of identified origin to be studied in long-term cultures. J. Cell Biol. 1986, 103:171-187.
29. Immke D.C., McCleskey E.W. Lactate enhances the acid-sensing Na+ channel on ischemia-sensing neurons. Nat. Neurosci. 2001, 4:869-870.
30. Immke D.C., McCleskey E.W. Protons open acid-sensing ion channels by catalyzing relief of Ca2+ blockade. Neuron 2003, 37:75-84.
31. Issberner U., Reeh P.W., Steen K.H. Pain due to tissue acidosis: a mechanism for inflammatory and ischemic myalgia?. Neurosci. Lett. 1996, 208:191-194.
32. Jasti J., Furukawa H., Gonzales E.B., Gouaux E. Structure of acid-sensing ion channel 1 at 1.9 A resolution and low pH. Nature 2007, 449:316-323.
33. Kaufman M.P., Hayes S.G. The Exercise Pressor Reflex. Clin. Auton. Res. 2002, 12:429.
34. Kawate T., Michel J.C., Birdsong W.T., Gouaux E. Crystal structure of the ATP-gated P2X(4) ion channel in the closed state. Nature 2009, 460:592-598.
35. Khakh B.S., Zhou X., Sydes J., Galligan J.J., Lester H.A. State-dependent cross-inhibition between transmitter-gated cation channels. Nature 2000, 406:405-410.
36. Khakh B.S., Fisher J.A., Nashmi R., Bowser D.N., Lester H.A. An angstrom scale interaction between plasma membrane ATP-gated P2X2 and alpha4beta2 nicotinic channels measured with fluorescence resonance energy transfer and total internal reflection fluorescence microscopy. J. Neurosci. 2005, 25:6911-6920.
37. Kobayashi K., Fukuoka T., Yamanaka H., Dai Y., Obata K., Tokunaga A., Noguchi K. Differential expression patterns of mRNAs for P2X receptor subunits in neurochemically characterized dorsal root ganglion neurons in the rat. J. Comp. Neurol. 2005, 481:377-390.
38. Lewis C., Neidhart S., Holy C., North R.A., Buell G., Surprenant A. Coexpression of P2X2 and P2X3 receptor subunits can account for ATP-gated currents in sensory neurons. Nature 1995, 377:432-435.
39. Lewis T. Pain in muscular ischemia: its relation to anginal pain. Arch. Intern. Med. 1932, 49:713-727.
40. Light A.R., Hughen R.W., 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.
41. Lingueglia E. Acid-sensing ion channels in sensory perception. J. Biol. Chem. 2007, 282:17325-17329.
42. Longhurst J.C., Tjen-A-Looi S.C., Fu L.-W. Cardiac sympathetic afferent activation provoked by myocardial ischemia and reperfusion. Mechanisms and reflexes. Ann. N. Y. Acad. Sci. 2001, 940:74-95.
43. MacWilliam J.A., Webster W.J. Some applications of physiology to medicine: 1.-Sensory phenomena associated with defective blood supply to working muscles. BMJ 1923, 1:51-53.
44. McCord J.L., Tsuchimochi H., Kaufman M.P. Acid-sensing ion channels contribute to the metaboreceptor component of the exercise pressor reflex. Am. J. Physiol. Heart Circ. Physiol. 2009, 297:H443-H449.
45. Meller S.T., Gebhart G.F. A critical review of the afferent pathways and the potential chemical mediators involved in cardiac pain. Neuroscience 1992, 48:501-524.
46. Mense S. Nociception from skeletal muscle in relation to clinical muscle pain. Pain 1993, 54:241-289.
47. Mense S. Muscle pain: mechanisms and clinical significance. Dtsch. Arztebl. Int. 2008, 105:214-219.
48. Molliver D.C., Immke D.C., Fierro L., Pare M., Rice F.L., McCleskey E.W. ASIC3, an acid-sensing ion channel, is expressed in metaboreceptive sensory neurons. Mol. Pain 2005, 1:35.
49. Nakazawa K. ATP-activated current and its interaction with acetylcholine-activated current in rat sympathetic neurons. J. Neurosci. 1994, 14:740-750.
50. North R.A., Surprenant A. Pharmacology of cloned P2X receptors. Annu. Rev. Pharmacol. Toxicol. 2000, 40:563-580.
51. Ormo M., Cubitt A.B., Kallio K., Gross L.A., Tsien R.Y., Remington S.J. Crystal structure of the Aequorea victoria green fluorescent protein. Science 1996, 273:1392-1395.
52. Pan H.L., Longhurst J.C., Eisenach J.C., Chen S.R. Role of protons in activation of cardiac sympathetic C-fibre afferents during ischaemia in cats. J. Physiol. 1999, 518:857-866.
53. Petroff E.Y., Price M.P., Snitsarev V., Gong H., Korovkina V., Abboud F.M., Welsh M.J. Acid-sensing ion channels interact with and inhibit BK K+ channels. Proc. Natl. Acad. Sci. USA 2008, 105:3140-3144.
54. Pratt E.B., Brink T.S., Bergson P., Voigt M.M., Cook S.P. Use-dependent inhibition of P2X3 receptors by nanomolar agonist. J. Neurosci. 2005, 25:7359-7365.
55. Rose B.D., Post T.W. Clinical Physiology of Acid-Base and Electrolyte Disorders 2001, McGraw-Hill, Medical Publishing Division, New York. Fifth Edition.
56. Runnels L.W., Yue L., Clapham D.E. TRP-PLIK, a bifunctional protein with kinase and ion channel activities. Science 2001, 291:1043-1047.
57. Ryten M., Dunn P.M., Neary J.T., Burnstock G. ATP regulates the differentiation of mammalian skeletal muscle by activation of a P2X5 receptor on satellite cells. J. Cell Biol. 2002, 158:345-355.
58. Seo H.S., Roh D.H., Yoon S.Y., Kang S.Y., Moon J.Y., Kim H.W., Han H.J., Chung J.M., Beitz A.J., Lee J.H. Peripheral acid-sensing ion channels and P2X receptors contribute to mechanical allodynia in a rodent thrombus-induced ischemic pain model. J. Pain. 2010, 11:718-727.
59. Sluka K.A., Price M.P., Breese N.M., Stucky C.L., Wemmie J.A., Welsh M.J. Chronic hyperalgesia induced by repeated acid injections in muscle is abolished by the loss of ASIC3, but not ASIC1. Pain 2003, 106:229-239.
60. Sluka K.A., Radhakrishnan R., Benson C.J., Eshcol J.O., Price M.P., Babinski K., Audette K.M., Yeomans D.C., Wilson S.P. ASIC3 in muscle mediates mechanical, but not heat, hyperalgesia associated with muscle inflammation. Pain 2007, 129:102-112.
61. Smith G.M., Egbert L.D., Markowitz R.A., Mosteller F., Beecher H.K. An experimental pain method sensitive to morphine in man: the submaximum effort tourniquet technique. J. Pharmacol. Exp. Ther. 1966, 154:324-332.
62. Steen K.H., Issberner U., Reeh P.W. Pain due to experimental acidosis in human skin: evidence for non-adapting nociceptor excitation. Neurosci. Lett. 1995, 199:29-32.
63. Street D., Bangsbo J., Juel C. Interstitial pH in human skeletal muscle during and after dynamic graded exercise. J. Physiol. 2001, 537:993-998.
64. Sutherland S.P., Benson C.J., Adelman J.P., McCleskey E.W. Acid-sensing ion channel 3 matches the acid-gated current in cardiac ischemia-sensing neurons. Proc. Natl. Acad. Sci. USA 2001, 98:711-716.
65. Ursell T., Huang K.C., Peterson E., Phillips R. Cooperative gating and spatial organization of membrane proteins through elastic interactions. PLoS Comput. Biol. 2007, 3:e81.
66. Vissing J., MacLean D.A., Vissing S.F., Sander M., Saltin B., Haller R.G. The exercise metaboreflex is maintained in the absence of muscle acidosis: insights from muscle microdialysis in humans with McArdle's disease. J. Physiol. 2001, 537:641-649.
67. Vulchanova L., Arvidsson U., Riedl M., Wang J., Buell G., Surprenant A., North R.A., Elde R. Differential distribution of two ATP-gated channels (P2X receptors) determined by immunocytochemistry. Proc. Natl. Acad. Sci. USA 1996, 93:8063-8067.
68. 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.
69. Weibel E. Stereological Methods. Practical Methods for Biological Morphometry 1979, Volume 1. Academic Press, London.
70. Wemmie J.A., Price M.P., Welsh M.J. Acid-sensing ion channels: advances, questions and therapeutic opportunities. Trends Neurosci. 2006, 29:578-586.
71. Wenk H.N., McCleskey E.W. A novel mouse skeletal muscle-nerve preparation and in vitro model of ischemia. J. Neurosci. Methods 2007, 159:244-251.
72. Xiong Z.G., Zhu X.M., Chu X.P., Minami M., Hey J., Wei W.L., MacDonald J.F., Wemmie J.A., Price M.P., Welsh M.J., Simon R.P. Neuroprotection in ischemia: blocking calcium-permeable acid-sensing ion channels. Cell 2004, 118:687-698.
73. Yagi J., Wenk H.N., Naves L.A., McCleskey E.W. Sustained Currents Through ASIC3 Ion Channels at the Modest pH Changes That Occur During Myocardial Ischemia. Circ. Res. 2006, 99:501-509.
74. Zhou X., Galligan J.J. Non-additive interaction between nicotinic cholinergic and P2X purine receptors in guinea-pig enteric neurons in culture. J. Physiol. 1998, 513:685-697.