Acid-evoked currents in cardiac sensory neurons: A possible mediator of myocardial ischemic sensation

Circulation Research

Volumn 84, Issue 8, 1999, Pages 921-928

  Benson, Christopher J ^a   Eckert, Stephani P ^a   McCleskey, Edwin W ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Cardiac sensory neuron; Myocardial ischemia; Proton; Whole cell patch clamp

Indexed keywords

ION CHANNEL;

ANGINA PECTORIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTONOMIC NERVOUS SYSTEM; EVOKED RESPONSE; HEART DEPOLARIZATION; HEART INNERVATION; HEART MUSCLE ISCHEMIA; NONHUMAN; PATHOGENESIS; PH; PRIORITY JOURNAL; RAT; SENSORY NERVE CELL; SPINAL GANGLION;

EID: 0033617361     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.84.8.921     Document Type: Article

References (55)

1. Cutler EC. Summary of experiences up-to-date in the surgical treatment of angina pectoris. Am J Med Sci. 1927;173:613-624.
2. White JC. Cardiac pain: anatomic pathways and physiologic mechanisms. Circulation. 1957;16:644-655.
3. Berry M, Bannister LH, Standering SM, eds. Gray's Anatomy. New York, NY: Churchill Livingstone; 1995;901-1397.
4. McNeill DL, Burden HW. Convergence of sensory processes from the heart and left ulnar nerve onto a single afferent perikaryon: a neuroanatomical study in the rat employing fluorescent tracers. Anat Rec. 1986; 214:441-444.
5. Lewis T. Pain in muscular ischemia: its relation to anginal pain. Arch Int Med. 1932;49:713-727.
6. Brown AM. Excitation of afferent cardiac sympathetic nerve fibres during myocardial ischemia. J Physiol (Lond). 1967;190:35-53.
7. Minisi AJ, Thames MD. Activation of cardiac sympathetic afferents during coronary occlusion: evidence for reflex activation of sympathetic nervous system during transmural myocardial ischemia in the dog. Circulation. 1991;84:357-367.
8. Huang MH, Horackova M, Negoescu RM, Wolf S, Armour JA. Polysensory response characteristics of dorsal root ganglion neurones that may serve sensory functions during myocardial ischaemia. Cardiovasc Res. 1996;32:503-515.
9. Thames MD, Klopfenstein HS, Abboud FM, Allyn LM, Walker JL. 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. 1978;43:512-519.
10. Armour JA, Huang MH, Pelleg A, Sylven C. Responsiveness of in situ canine nodose ganglion afferent neurones to epicardial mechanical or chemical stimuli. Cardiovasc Res. 1994;28:1218-1225.
11. James TN. A cardiogenic hypertensive chemoreflex. Anesth Analg. 1989; 69:633-646.
12. Baker DG, Coleridge HM, Coleridge JCG, Nerdrum T. Search for a cardiac nociceptor: stimulation by bradykinin of sympathetic afferent nerve endings in the heart of the cat. J Physiol (Lond). 1980;306: 519-536.
13. Euchner-Wamser I, Meller ST, Gebhart GF. A model of cardiac nociception in chronically instrumented rats: behavioral and electrophysiological effects of pericardial administration of algogenic substances. Pain. 1994;58:117-128.
14. Malliani A, Schwartz PJ, Zanchetti A. A sympathetic reflex elicited by experimental coronary occlusion. Am J Physiol. 1969;217:703-709.
15. Sleight P. A cardiovascular depressor reflex from the epicardium of the left ventricle in the dog. J Physiol (Lond). 1964;173:321-343.
16. Meiler ST, Gebhart GF. A critical review of the afferent pathways and the potential chemical mediators involved in cardiac pain. Neuroscience. 1992;48:501-524.
17. Jacobus WE, Taylor GT IV, Hollis DP, Nunnally RL. Phosphorus nuclear magnetic resonance of perfused working rat hearts. Nature. 1977;265: 756-758.
18. Cobbe SM, Poole-Wilson PA. The time of onset and severity of acidosis in myocardial ischemia. J Mol Cell Cardiol. 1980;12:745-760.
19. + increase and noradrenaline release as possible cause of early arrhythmias following acute coronary artery occlusion in pigs. J Mol Cell Cardiol. 1980;12:579-593.
20. Cobbe SM, Poole-Wilson PA. Continuous coronary sinus and arterial pH monitoring during pacing-induced ischaemia in coronary artery disease. Br Heart J. 1982;47:369-374.
21. Uchida Y, Murao S. Acid-induced excitation of afferent cardiac sympathetic nerve fibers. Am J Physiol. 1975;228:27-33.
22. Steen KH, Steen AE, Reeh PW. A dominant role of acid pH in inflammatory excitation and sensitization of nociceptors in rat skin, in vitro. J Neurosci. 1995;15:3982-3989.
23. Krishtal OA, Pidoplichko VI. A receptor for protons in the nerve cell membrane. Neuroscience. 1980;5:2325-2327.
24. Konnerth A, Lux HD, Morad M. Proton-induced transformation of calcium channel in chick dorsal root ganglion cells. J Physiol [Lond). 1987;386:603-633.
25. Davies NW, Lux HD, Morad M. Site and mechanism of activation of proton-induced sodium current in chick dorsal root ganglion neurons. J Physiol (Lond). 1988;400:159-187.
26. Bevan S, Yeats J. Protons activate a cation conductance in a subpopulation of rat dorsal root ganglion neurones. J Physiol (Lond). 1991; 433:145-161.
27. Krishtal OA, Pidoplichko VI. A receptor for protons in the membrane of sensory neurons may participate in nociception. Neuroscience. 1981;6: 2599-2601.
28. +-gated cation channels: neuronal acid sensors in the NaC/DEG family of ion channels. Curr Opin Neurobiol. 1998;8:418-424.
29. Nakatani T, Shinohara H, Fukuo Y, Morisawa S, Matsuda T. Pericardium of rodents: pores connect the pericardial and pleural cavities. Anat Rec. 1988;220:132-137.
30. Eckert SP, Taddese A, McCleskey EW. Isolation and culture of rat sensory neurons having distinct sensory modalities. J Neurosci Methods. 1997;77:183-190.
31. Hille B. Selective permeability: independence. In: Ion Channels of Excitable Membranes. Sunderland, Mass: Sinauer Associates; 1992: 344-347.
32. Cook SP, Vulchanova L, Hargreaves KM, Elde R, McCleskey EW. Distinct ATP receptors on pain-sensing and stretch-sensing neurons. Nature. 1997;387:505-508.
33. 3 receptor, a serotonin-gated ion channel. Science. 1991;254:432-436.
34. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature. 1997;389:816-824.
35. Sucher NJ, Cheng TPO, Lipton SA. Neural nicotinic acetylcholine responses in sensory neurons from postnatal rat. Brain Res. 1990;533: 248-254.
36. 2 of bradykinin activation of embryonic rat sensory neurones. J Physiol (Lond). 1994;480: 485-492.
37. Allen TGJ, Burnstock G. The actions of adenosine 5′-triphosphate on guinea-pig intracardiac neurones in culture. Br J Pharmacol. 1990;100: 269-276.
38. 3 receptor subunits can account for ATP-gated currents in sensory neurons. Nature. 1995;377:432-435.
39. Chen CC, Akopian AN, Sivilotti L, Colquhoun D, Burnstock G, Wood JN. A P2X purinoceptor expressed by a subset of sensory neurons. Nature. 1995;377:428-431.
40. Kovalchuk YN, Krishtal OA, Nowycky MC. The proton-activated inward current of rat sensory neurons includes a calcium component. Neurosci Lett. 1990;115:237-242.
41. Waldmann R, Champigny G, Bassilana F, Heurteaux C, Lazdunski M. A proton-gated cation channel involved in acid-sensing. Nature. 1997;386: 173-177.
42. Tang CM, Presser F, Morad M. Amiloride selectively blocks the low threshold (T) calcium channel. Science. 1988;240:213-215.
43. + channel specific for sensory neurons. J Biol Chem. 1997;272: 20975-20978.
44. + channel is made of three homologous subunits. Nature. 1994;367:463-467.
45. Alles A, Dom RM. Peripheral sensory nerve fibers that dichotomize to supply the brachium and the pericardium in the rat: a possible morphological explanation for referred cardiac pain? Brain Res. 1985;342: 382-385.
46. Bevan S, Winter J. Nerve growth factor (NGF) differentially regulates the chemosensitivity of adult rat cultured sensory neurons. J Neurosci. 1995; 15:4918-4926.
47. Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H, Skinner K, Raumann BE, Basbaum AI, Julius D. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron. 1998;21:531-543.
48. Deanfield JE, Shea MJ, Selwyn AP. Clinical evaluation of transient myocardial ischemia during daily life. Am J Med. 1985;79(suppl 3A): 18-24.
49. Malliani A. Significance of experimental models in assessing the link between myocardial ischemia and pain. Adv Cardiol. 1990;37:126-141.
50. Rosen SD, Paulesu E, Nihoyannopoulos P, Tousoulis D, Prackowiak SJ, Frith CD, Jones T, Camici PG. Silent ischemia as a central problem: regional brain activation compared in silent and painful myocardial ischemia. Ann Intern Med. 1996;124:939-949.
51. Thamer V, Deussen A, Schipke JD, Tolle T, Heusch G. Pain and myocardial ischemia: the role of sympathetic activation. Basic Res Cardiol. 1990;85:253-266.
52. Francis GS, Goldsmith SR, Levine TB, Olivari MT, Cohn JN. The neurohormonal axis in congestive heart failure. Ann Intern Med. 1984; 101:370-377.
53. Mitrani RD, Zipes DP. Clinical neurocardiology: arrhythmias. In: Armour JA, Ardell JL, ed. Neurocardiology. New York, NY: Oxford University Press; 1994:365-395.
54. Victor RG, Bertocci LA, Pryor SL, Nunnally RL. Sympathetic nerve discharge is coupled to muscle cell pH during exercise in humans. J Clin Invest. 1988;82:1301-1305.
55. Rendig SV, Chalal PS, Longhurst JC. Cardiovascular reflex responses to ischemia during occlusion of celiac and/or superior mesenteric arteries. Am J Physiol. 1997;272:H791-H796.