ASICs function as cardiac lactic acid sensors during myocardial ischemia

Molecular Sensors for Cardiovascular Homeostasis

Volumn , Issue , 2007, Pages 32-50

  Benson, Christopher J ^a   McCleskey, Edwin W ^b  

^a UNIVERSITY OF IOWA   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 78449273054     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-0-387-47530-1_2     Document Type: Chapter

References (100)

1. The World Health Report, 2002. WHO Press.
2. Gibbons, R.J., Abrams, J., Chatterjee, K., Daley, J., Deedwania, P.C., Douglas, J.S., Ferguson, T.B., Jr., Fihn, S.D., Fraker, T.D., Jr., Gardin, J.M., O'Rourke, R.A., Pasternak, R.C., Williams, S.V., Alpert, J.S., Antman, E.M., Hiratzka, L.F., Fuster, V., Faxon, D.P., Gregoratos, G., Jacobs, A.K., and Smith, S.C., Jr., ACC/AHA 2002 guideline update for the management of patients with chronic stable angina- summary article: A report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (Committee on the Management of Patients With Chronic Stable Angina), Circulation. 107, 149-58 (2003).
3. Cutler, E.C., Summary of experiences up-to-date in the surgical treatment of angina pectoris., Am. J. Med. Sci. 173, 613-624 (1927).
4. Lingren, I., and Olivecrona, H., Surgical treatment of angina pectoris, J. Neurosurg. 4, 19-39 (1947).
5. White, J.C., Cardiac pain: anatomic pathways and physiologic mechanisms, Circulation. 16, 644-655 (1957).
6. Kuo, D.C., Oravitz, J.J., and DeGroat,W.C.,Tracing of afferent and efferent pathways in the left inferior cardiac nerve of the cat using retrograde and transganglionic transport of horseradish peroxidase, Brain Res. 321, 111-118. (1984).
7. Meller, S.T., and Gebhart, G.F., A critical review of the afferent pathways and the potential chemical mediators involved in cardiac pain, Neuroscience. 48, 501-24 (1992).
8. Thames, M.D., Klopfenstein, H.S., Abboud, F.M., Mark, A.L., and Walker, J.L., Preferential distribution of inhibitory cardiac receptors with vagal afferents to the inferoposterior wall of the left ventricle activated during coronary occlusion in the dog, Circ. Res. 43, 512-19 (1978).
9. Miller, M.R., and Kasahara, M., Studies on the nerve endings in the heart, Am J Anat. 115, 217-33 (1964).
10. Barber, M.J., Mueller, T.M., Davies, B.G., and Zipes, D.P., Phenol topically applied to canine left ventricular epicardium interrupts sympathetic but not vagal afferents, Circ. Res. 55, 532-44 (1984).
11. Huang, H.S., Pan, H.L., Stahl, G.L., Longhurst, J.C., Ischemia- and reperfusionsensitive cardiac sympathetic afferents: influence of H2O2 and hydroxyl radicals, Am. J. Physiol. 269, H888-901 (1995).
12. Pan, H.L., and Chen, S.R., Myocardial ischemia recruits mechanically insensitive cardiac sympathetic afferents in cats, J. Neurophysiol. 87, 660-8 (2002).
13. Huang, M.H., Horackova, M., Negoescu, R.M., Wolf, S., and Armour, J.A., Polysensory response characteristics of dorsal root ganglion neurones that may serve sensory functions during myocardial ischaemia, Cardiovasc. Res. 32, 503-15 (1996).
14. Malliani, A., The elusive link between transient myocardial ischemia and pain, Circulation. 73, 201-4 (1986).
15. Cervero, F., and Janig,W.,Visceral nociceptors: a newworld order?, Trends Neurosci. 15, 374-8 (1992).
16. Colbeck, E.H., Angina pectoris: a criticism and a hypothesis, Lancet. 1, 793-95 (1903).
17. Davies, G.J., Bencivelli, W., Fragasso, G., Chierchia, S., Crea, F., Crow, J., Crean, P.A., Pratt, T., Morgan, M., and Maseri, A., Sequence and magnitude of ventricular volume changes in painful and painless myocardial ischemia, Circulation. 78, 310-9 (1988).
18. Lewis, T., Pain in muscular ischemia: its relation to anginal pain, Arch. Int. Med. 49, 713-27 (1932).
19. Baker, D.G., Coleridge, H.M., Coleridge, J.C., and Nerdrum, T., Search for a cardiac nociceptor: stimulation by bradykinin of sympathetic afferent nerve endings in the heart of the cat, J. Physiol. (Lond). 306, 519-36 (1980).
20. Lombardi, F., Della Bella, P., Casati, R., and Malliani, A., Effects of intracoronary administration of bradykinin on the impulse activity of afferent sympathetic unmyelinated fibers with left ventricular endings in the cat, Circ. Res. 48, 69-75 (1881).
21. Thames, M.D., Kinugawa, T., and Dibner-Dunlap, M.E., Reflex sympathoexcitation by cardiac sympathetic afferents during myocardial ischemia. Role of adenosine, Circulation. 87, 1698-704 (1993).
22. James, T.N., A cardiogenic hypertensive chemoreflex, Anesth. Analg. 69, 633-46 (1989).
23. Nishi, K., Sakanashi, M., and Takenaka, F., Activation of afferent cardiac sympathetic nerve fibers of the cat by pain-producing substances and by noxious heat, Pflugers Arch. 372, 53-61 (1977).
24. Armour, J.A., Huang, M.H., Pelleg, A., Sylven, C., Responsiveness of in situ canine nodose ganglion afferent neurones to epicardial mechanical or chemical stimuli, Cardiovasc. Res. 28, 1218-25 (1994).
25. Ustinova, E.E., and Schultz, H.D., Activation of cardiac vagal afferents in ischemia and reperfusion: Prostaglandins versus oxygen-derived free radicals, Circ. Res. 74, 904-11 (1994).
26. Ustinova, E.E., and Schultz, H.D., Activation of cardiac vagal afferents by oxygenderived free radicals in rats, Circ. Res. 74, 895-903 (1994).
27. Uchida, Y., and Murao, S., Acid-induced excitation of afferent cardiac sympathetic nerve fibers, Am. J. Physiol. 228, 27-33 (1975).
28. Pan, H.L., Longhurst, J.C., Eisenach, J.C., and Chen, S.R., Role of protons in activation of cardiac sympathetic C-fibre afferents during ischaemia in cats, J. Physiol. (Lond). 518, 857-66 (1999).
29. Vaughan-Jones, R.D., Eisner, D.A., and Lederer,W.J., Effects of changes of intracellular pH on contraction in sheep cardiac Purkinje fibers, J. Gen. Physiol. 89, 1015-32 (1987).
30. Halestrap, A.P.,Wang, X., Poole, R.C., Jackson, V.N., and Price, N.T., Lactate transport in heart in relation to myocardial ischemia, Am. J. Cardiol. 80, 17A-25A (1997).
31. Jacobus, W.E., Taylor, G.J.I., Hollis, D.P., and Nunnally, R.L., Phosphorus nuclear magnetic resonance of perfused working rat hearts, Nature. 265, 756-58 (1977).
32. Yan, G.X., and Kleber, A.G., Changes in extracellular and intracellularpHin ischemic rabbit papillary muscle, Circ. Res. 71, 460-70 (1992).
33. Hirsch, H.J., Franz, C.H.R., Bos, L., Bissig, R., Lang, R., and Schramm, M., Myocardial extracellular K+ and H+ increase and noradrenaline release as possible cause of early arrhythmias following acute coronary artery occlusion in pigs, J. Mol. Cell Cardiol. 12, 579-93 (1980).
34. Cobbe, S.M., and Poole-Wilson, P.A., The time of onset and severity of acidosis in myocardial ischaemia, J. Mol. Cell Cardiol. 12, 745-60 (1980).
35. Remme, W.J., van den Berg, R., Mantel, M., Cox, P.H., van Hoogenhuyze, D.C., Krauss, X.H., Storm, C.J., and Kruyssen, D.A., Temporal relation of changes in regional coronary flow and myocardial lactate and nucleoside metabolism during pacing-induced ischemia, Am. J. Cardiol. 58, 1188-94 (1986).
36. Sylven, C., Angina pectoris: Clinical characteristics, neurophysiological and molecular mechanisms, Pain. 36, 145-67 (1989).
37. Kress, M., and Reeh, P.W., More sensory competence for nociceptive neurons in culture, Proc. Natl. Acad. Sci. USA. 93, 14995-97 (1996).
38. Benson, C.J., Eckert, S.P., and McCleskey, E.W., Acid-evoked currents in cardiac sensory neurons: A possible mediator of myocardial ischemic sensation, Circ. Res. 84, 921-28 (1999).
39. Krishtal, O.A., and Pidoplichko, V.I., Receptor for protons in the membrane of sensory neurons, Brain Res. 214, 150-54 (1981).
40. Krishtal, O.A., and Pidoplichko, V.I., A receptor for protons in the membrane of sensory neurons may participate in nociception, Neuroscience. 6, 2599-601 (1981).
41. Bevan, S., and Yeats, J., Protons activate a cation conductance in a subpopulation of rat dorsal root ganglion neurones, J. Physiol. (Lond). 433, 145-61 (1991).
42. Caterina, M.J., Schumacher, M.A., Tominaga, M., Rosen, T.A., Levine, J.D., and Julius, D., The capsaicin receptor: a heat-activated ion channel in the pain pathway, Nature. 389, 816-24 (1997).
43. Caterina, M.J., Leffler, A., Malmberg, A.B., Martin,W.J., Trafton, J., Petersen-Zeitz, K.R., Koltzenburg, M., Basbaum, A.I., and Julius, D., Impaired nociception and pain sensation in mice lacking the capsaicin receptor [see comments], Science. 288, 306-13 (2000).
44. Davis, J.B., Gray, J., Gunthorpe, M.J., Hatcher, J.P., Davey, P.T., Overend, P., Harries, M.H., Latcham, J., Clapham, C., Atkinson, K., Hughes, S.A., Rance, K., Grau, E., Harper, A.J., Pugh, P.L., Rogers, D.C., Bingham, S., Randall, A., and Sheardown, S.A.,Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia, Nature. 405, 183-7 (2000).
45. Tominaga, M., Caterina, M.J., Malmberg, A.B., Rosen, T.A., Gilbert, H., Skinner, K., Raumann, B.E., Basbaum, A.I., and Julius, D., The cloned capsaicin receptor integrates multiple pain-producing stimuli [see comments], Neuron. 21, 531-43 (1998).
46. Zygmunt, P.M., Petersson, J., Andersson, D.A., Chuang, H., Sorgard, M., Di Marzo, V., Julius, D., and Hogestatt, E.D., Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide, Nature. 400, 452-57 (1999).
47. Voets, T., Droogmans, G.,Wissenbach, U., Janssens, A., Flockerzi,V., Nilius, B., The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels, Nature. 430, 748-54 (2004).
48. Garty, H., Palmer, L.G., Epithelial sodium channels: function, structure, and regulation, Physiol. Rev. 77, 359-96 (1997).
49. Tavernarakis, N., and Driscoll, M., Molecular modeling of mechanotransduction in the nematode Caenorhabditis elegans, Annu. Rev. Physiol. 59, 659-89 (1997).
50. Waldmann, R., Champigny, G., Bassilana, F., Heurteaux, C., and Lazdunski, M., A proton-gated cation channel involved in acid-sensing, Nature. 386, 173-77 (1997).
51. Garcia-Anoveros, J., Derfler, B., Neville-Golden, J., Hyman, B.T., and Corey, D.P., BNaC1 and BNaC2 constitute a new family of human neuronal sodium channels related to degenerins and epithelial sodium channels, Proc. Natl. Acad. Sci. USA. 94, 1459-64 (1997).
52. Price, M.P., Snyder, P.M., andWelsh, M.J., Cloning and expression of a novel human brain Na+ channel, J. Biol. Chem. 271, 7879-82 (1996).
53. Waldmann, R., Bassilana, F., de Weille, J., Champigny, G., Heurteaux, C., and Lazdunski, M., Molecular cloning of a non-inactivating proton-gated Na+ channel specific for sensory neurons, J. Biol. Chem. 272, 20975-78 (1997).
54. Akopian, A.N., Chen, C.C., Ding, Y., Cesare, P., and Wood, J.N., A new member of the acid-sensing ion channel family, Neuroreport. 11, 2217-22 (2000).
55. Grunder, S., Geissler, H.S., Bassler, E.L., and Ruppersberg, J.P., A new member of acid-sensing ion channels from pituitary gland, Neuroreport. 11, 1607-11 (2000).
56. Lingueglia, E., de Weille, J.R., Bassilana, F., Heurteaux, C., Sakai, H., Waldmann, R., and Lazdunski, M., A modulatory subunit of acid-sensing ion channels in brain and dorsal root ganglion cells, J. Biol. Chem. 272, 29778-83 (1997).
57. Bassilana, F., Champigny, G., Waldmann, R., de Weille, J.R., Heurteaux, C., and 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. 272, 28819-22 (1997).
58. 3+, J. Biol. Chem. 275, 28519-25 (2000).
59. +-gated cation channels: neuronal acid sensors in the NaC/DEG family of ion channels, Curr. Opin. Neurobiol. 8, 418-24 (1998).
60. Chen, C.C., England, S., Akopian, A.N., andWood, J.N., A sensory neuron-specific, proton-gated ion channel, Proc. Natl. Acad. Sci. USA. 95, 10240-45 (1998).
61. Price, M.P., Lewin, G.R., McIlwrath, S.L., Cheng, C., Xie, J., Heppenstall, P.A., Stucky, C.L., Mannsfeldt, A.G., Brennan, T.J., Drummond, H.A., Qiao, J., Benson, C.J., Tarr, D.E., Hrstka, R.F., Yang, B., Williamson, R.A., and Welsh, M.J., The mammalian sodium channel BNC1 is required for normal touch sensation, Nature. 407, 1007-11 (2000).
62. Garcia-Anoveros, J., Samad, T.A., Woolf, C.J., and Corey, D.P., Transport and localization of the DEG/ENaC ion channel BNaC1a to peripheral mechanosensory terminals of dorsal root ganglia neurons, J. Neurosci. 21, 2678-86 (2001).
63. Price, M.P., McIlwrath, S.L., Xie, J., Cheng, C., Qiao, J., Tarr, D.E., Sluka, K.A., Brennan, T.J., Lewin, G.R., andWelsh, M.J., The DRASIC cation channel contributes to the detection of cutaneous touch and acid stimuli in mice, Neuron. 32, 1071-83 (2001).
64. Krishtal, O.A., and Pidoplichko, V.I., A receptor for protons in the nerve cell membrane, Neuroscience. 5, 2325-27 (1980).
65. Zahner, M.R., Li, D.P., Chen, S.R., and Pan, H.L., Cardiac vanilloid receptor 1- expressing afferent nerves and their role in the cardiogenic sympathetic reflex in rats, J. Physiol. 551, 515-23. Epub 2003 Jun 26 (2003).
66. Pan, H.L., and Chen, S.R., Sensing tissue ischemia: another new function for capsaicin receptors?, Circulation. 110, 1826-31. Epub 2004 Sep 13 (2004).
67. Sutherland, S.P., Benson, C.J., Adelman, J.P., and McCleskey, E.W., Acid-sensing ion channel 3 matches the acid-gated current in cardiac ischemia-sensing neurons, Proc. Natl. Acad. Sci. USA. 98, 711-716 (2001).
68. Benson, C.J., Xie, J., Wemmie, J.A., Price, M.P., Henss, J.M., Welsh, M.J., and Snyder, P.M., Heteromultimers of DEG/ENaC subunits form H+-gated channels in mouse sensory neurons, Proc. Natl. Acad. Sci. USA. 99, 2338-43 (2002).
69. Stahl, G.L., and Longhurst, J.C., Ischemically sensitive visceral afferents: importance ofH+derived from lactic acid and hypercapnia, Am. J. Physiol. 262, H748-53 (1992).
70. Hong, J.L., Kwong, K., and Lee, L.Y., Stimulation of pulmonary C fibres by lactic acid in rats: contributions of H+ and lactate ions, J. Physiol. 500, 319-29 (1997).
71. Cohen, R., and Woods, H., Lactic acidosis revisited, Diabetes. 32, 181-91 (1983).
72. Aresta, F., Gerstenblith, G., and Weiss, R.G., Repeated, transient lactate exposure does not "precondition" rat myocardium, Can. J. Physiol. Pharmacol. 75, 1262-66 (1997).
73. + channel on ischemia-sensing neurons, Nat. Neurosci. 4, 869-70 (2001).
74. Immke, D.C., and McCleskey, E.W., Protons open acid-sensing ion channels by catalyzing relief of Ca2+ blockade, Neuron. 37, 75-84 (2003).
75. Euchner-Wamser, I., Meller, S.T., and Gebhart, G.F., A model of cardiac nociception in chronically instrumented rats: behavioral and electrophysiological effects of pericardial administration of algogenic substances, Pain. 58, 117-28 (1994).
76. Kessler, W., Kirchhoff, C., Reeh, P.W., and Handwerker, H.O., Excitation of cutaneous afferent nerve endings in vitro by a combination of inflammatory mediators and conditioning effect of substance P, Exp. Brain Res. 91, 467-76 (1992).
77. Steen, K.H., Steen, A.E., and Reeh, P.W.,Adominant role of acid pH in inflammatory excitation and sensitization of nociceptors in rat skin, in vitro, J. Neurosci. 15, 3982-89 (1995).
78. Mamet, J., Baron, A., Lazdunski, M., and Voilley, N., Proinflammatory mediators, stimulators of sensory neuron excitability via the expression of acid-sensing ion channels, J. Neurosci. 22, 10662-70 (2002).
79. Voilley, N., deWeille, J., Mamet, J., and Lazdunski, M., Nonsteroid anti-inflammatory drugs inhibit both the activity and the inflammation-induced expression of acidsensing ion channels in nociceptors, J. Neurosci. 21, 8026-33 (2001).
80. Mamet, J., Lazdunski, M., andVoilley, N., Hownerve growth factor drives physiological and inflammatory expressions of acid-sensing ion channel 3 in sensory neurons, J. Biol. Chem. 278, 48907-13. Epub 2003 Sep 30 (2003).
81. Deval, E., Salinas, M., Baron, A., Lingueglia, E., and Lazdunski, M., ASIC2bdependent regulation of ASIC3, an essential acid-sensing ion channel subunit in sensory neurons via the partner protein PICK-1, J. Biol. Chem. 279, 19531-9. Epub 2004 Feb 19 (2004).
82. Baron, A., Deval, E., Salinas, M., Lingueglia, E., Voilley, N., and Lazdunski, M., Protein kinaseCstimulates the acid-sensing ion channel ASIC2a via thePDZdomaincontaining protein PICK1, J. Biol Chem. 277, 50463-8. Epub 2002 Oct 23 (2002).
83. Burgess, G.M., Mullaney, I., McNeill, M., Dunn, P.M., and Rang, H.P., Second messengers involved in the mechanism of action of bradykinin in sensory neurons in culture, J. Neurosci. 9, 3314-25 (1989).
84. Barbas, D., DesGroseillers, L., Castellucci, V.F., Carew, T.J., and Marinesco, S., Multiple serotonergic mechanisms contributing to sensitization in aplysia: evidence of diverse serotonin receptor subtypes, Learn. Mem. 10, 373-86 (2003).
85. Nicholson, R., Small, J., Dixon, A.K., Spanswick, D., and Lee, K., Serotonin receptor mRNA expression in rat dorsal root ganglion neurons, Neurosci. Lett. 337, 119-22 (2003).
86. Leonard, A.S., Yermolaieva, O., Hruska-Hageman, A., Askwith, C.C., Price, M.P., Wemmie, J.A., and Welsh, M.J., 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. 100, 2029-34 (2003).
87. Aley, K.O., Levine, J.D., Role of protein kinaseAin the maintenance of inflammatory pain, J. Neurosci. 19, 2181-86 (1999).
88. Julius, D., and Basbaum, A.I., Molecular mechanisms of nociception, Nature. 413, 203-10 (2001).
89. Atzori, M., Lau, D., Tansey, E.P., Chow, A., Ozaita, A., Rudy, B., and McBain, C.J., H2 histamine receptor-phosphorylation of Kv3.2 modulates interneuron fast spiking, Nat. Neurosci. 3, 791-98 (2000).
90. England, S., Bevan, S., and Docherty, R.J.,PGE2modulates the tetrodotoxin-resistant sodium current in neonatal rat dorsal root ganglion neurons via the cyclic AMPprotein kinase A cascade, J. Physiol. 495, 429-40 (1996).
91. Taiwo, Y.O., Heller, P.H., and Levine, J.D., Mediation of serotonin hyperalgesia by the cAMP second messenger system, Neuroscience. 48, 479-83 (1992).
92. Taiwo, Y.O., and Levine, J.D., Direct cutaneous hyperalgesia induced by adenosine, Neuroscience. 38, 757-62 (1990).
93. Deanfield, J.E., Shea, M.J., and Selwyn, A.P., Clinical evaluation of transient myocardial ischemia during daily life, Am. J. Med. 79, 18-24 (1985).
94. Malliani, A., Significance of experimental models in assessing the link between myocardial ischemia and pain, Adv. Cardiol. 37, 126-41 (1990).
95. Rosen, S.D.,Paulesu, E., Nihoyannopoulos, P.,Tousoulis, D., Frackowiak, R.S., Frith, C.D., Jones, T., and Camici, P.G., Silent ischemia as a central problem: regional brain activation compared in silent and painful myocardial ischemia [see comments], Ann. Intern. Med. 124, 939-49 (1996).
96. Schang, S.J., Jr. and Pepine, C.J., Transient asymptomatic S-T segment depression during daily activity, Am. J. Cardiol. 39, 396-402 (1977).
97. Malliani, A., Schwartz, P.J., and Zanchetti, A., A sympathetic reflex elicited by experimental coronary occlusion, Am. J. Physiol. 217, 703-9 (1969).
98. Minisi, A.J., and Thames, M.D., Activation of cardiac sympathetic afferents during coronary occlusion: Evidence for reflex activation of sympathetic nervous system during transmural myocardial ischemia in the dog, Circulation. 84, 357-67 (1991).
99. Webb, S.W., Adgey, A.A., and Pantridge, J.F., Autonomic disturbance at onset of acute myocardial infarction, Br. Med. J. 3, 89-92 (1972).
100. Gottlieb, S.S., McCarter, R.J., and Vogel, R.A., Effect of beta-blockade on mortality among high-risk and low-risk patients after myocardial infarction, N. Engl. J. Med. 339, 489-97 (1998).