Differential distribution of voltage-gated channels in myelinated and unmyelinated baroreceptor afferents

Autonomic Neuroscience: Basic and Clinical

Volumn 172, Issue 1-2, 2012, Pages 4-12

  Schild, John H ^a   Kunze, Diana L ^b  

^a Indiana University Purdue University Indianapolis   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

Baroreceptor; Ion channels; Myelinated; Nodose; Unmyelinated

Indexed keywords

CALCIUM ACTIVATED CHANNEL KCAL1.1; HYPER POLARIZATION ACTIVATED CHANNEL HCN1; HYPER POLARIZATION ACTIVATED CHANNEL HCN2; HYPER POLARIZATION ACTIVATED CHANNEL HCN4; POTASSIUM CHANNEL KCNQ2; POTASSIUM CHANNEL KCNQ3; POTASSIUM CHANNEL KCNQ5; POTASSIUM CHANNEL KV1.1; POTASSIUM CHANNEL KV1.2; POTASSIUM CHANNEL KV1.3; POTASSIUM CHANNEL KV1.6; SODIUM CHANNEL NAV1.7; SODIUM CHANNEL NAV1.8; SODIUM CHANNEL NAV1.9; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED CALCIUM CHANNEL CAV1.2; VOLTAGE GATED CALCIUM CHANNEL CAV1.3; VOLTAGE GATED CALCIUM CHANNEL CAV2.1; VOLTAGE GATED POTASSIUM CHANNEL; VOLTAGE GATED POTASSIUM CHANNEL KV2.1; VOLTAGE GATED POTASSIUM CHANNEL KV2.2; VOLTAGE GATED SODIUM CHANNEL;

ACTION POTENTIAL; AFFERENT NERVE GROUP 1; DEPOLARIZATION; ELECTROPHYSIOLOGY; HYPERPOLARIZATION; MEMBRANE POTENTIAL; MEMBRANE STEADY POTENTIAL; MYELINATED NERVE; NERVE CELL EXCITABILITY; NERVE FIBER C; NEUROMODULATION; NONMYELINATED NERVE; PERIKARYON; PRESSORECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVIEW; SENSORY NERVE; VELOCITY; VOLTAGE CLAMP;

ANIMALS; ARTERIES; AUTONOMIC NERVOUS SYSTEM; BAROREFLEX; CALCIUM CHANNELS; HUMANS; NERVE FIBERS, MYELINATED; NERVE FIBERS, UNMYELINATED; NODOSE GANGLION; ORGAN SPECIFICITY; POTASSIUM CHANNELS, VOLTAGE-GATED; VOLTAGE-GATED SODIUM CHANNELS;

EID: 84870716485     PISSN: 15660702     EISSN: 18727484     Source Type: Journal    
DOI: 10.1016/j.autneu.2012.10.014     Document Type: Review

References (69)

1. Alfrey K.D., Li B.Y., Schild J.H. The Differential Role of the KCa Current upon Somatic Action Potential and Repetitive Discharge Properties of Myelinated and Unmyelinated Afferents from Rat Nodose Ganglia. Society for Neuroscience Abstract 501.15 2003.
2. Andresen M.C. Short- and long-term determinants of baroreceptor function in aged normotensive and spontaneously hypertensive rats. Circ. Res. 1984, 54:750-759.
3. Belmonte C., Gallego R. Membrane properties of cat sensory neurons with chemoreceptor and baroreceptor endings. J. Physiol. 1983, 342:603-614.
4. Blair N.T., Bean B.P. Roles of tetrodotoxin (TTX)-sensitive Na+ current, TTX-resistant Na+ current, and Ca2+ current in the action potentials of nociceptive sensory neurons. J. Neurosci. 2002, 22:10277-10290.
5. Bossu J.L., Feltz A. Patch-clamp study of the tetrodotoxin-resistant sodium current in group C sensory neurones. Neurosci. Lett. 1984, 51:241-246.
6. Cantrell A.R., Catterall W.A. Neuromodulation of Na+ channels: an unexpected form of cellular plasticity. Nat. Rev. Neurosci. 2001, 2:397-407.
7. Chapleau M.W., Li Z., Meyrelles S.S., Ma X., Abboud F.M. Mechanisms determining sensitivity of baroreceptor afferents in health and disease. Ann. N. Y. Acad. Sci. 2001, 940:1-19.
8. Chen J., Ikeda S.R., Lang W., Isales C.M., Wei X. Molecular cloning of a putative tetrodotoxin-resistant sodium channel from dog nodose ganglion neurons. Gene 1997, 202:7-14.
9. Cheng Z., Powley T.L., Schwaber J.S., Doyle F.J. A laser confocal microscopic study of vagal afferent innervation of rat aortic arch: chemoreceptors as well as baroreceptors. J. Auton. Nerv. Syst. 1997, 67:1-14.
10. Cohen C.J., McCarthy R.T. Nimodipine block of calcium channels in rat anterior pituitary cells. J. Physiol. 1987, 387:195-225.
11. Coleridge H.M., Coleridge J.C. Cardiovascular afferents involved in regulation of peripheral vessels. Annu. Rev. Physiol. 1980, 42:413-427.
12. Coleridge H.M., Coleridge J.C., Schultz H.D. Characteristics of C fibre baroreceptors in the carotid sinus of dogs. J. Physiol. 1987, 394:291-313.
13. Cordoba-Rodriguez R., Moore K.A., Kao J.P., Weinreich D. Calcium regulation of a slow post-spike hyperpolarization in vagal afferent neurons. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:7650-7657.
14. Coste B., Cres t M., Delmas P. Pharmacological dissection and distribution of NaN/Nav1.9, T-type Ca2+ currents, and mechanically activated cation currents in different populations of DRG neurons. J. Gen. Physiol. 2007, 129:57-77.
15. Doan T.N., Kunze D.L. Contribution of the hyperpolarization-activated current to the resting membrane potential of rat nodose sensory neurons. J. Physiol. 1999, 514:125-138.
16. Doan T.N., Stephans K., Ramirez A.N., Glazebrook P.A., Andresen M.C., Kunze D.L. Differential distribution and function of hyperpolarization-activated channels in sensory neurons and mechanosensitive fibers. J. Neurosci. 2004, 24:3335-3343.
17. Fan W., Andresen M.C. Differential frequency-dependent reflex integration of myelinated and nonmyelinated rat aortic baroreceptors. Am. J. Physiol. 1998, 275:H632-H640.
18. Fan W., Schild J.H., Andresen M.C. Graded and dynamic reflex summation of myelinated and unmyelinated rat aortic baroreceptors. Am. J. Physiol. 1999, 277:R748-R756.
19. Glazebrook P.A., Ramirez A.N., Schild J.H., Shieh C.C., Doan T., Wible B.A., Kunze D.L. Potassium channels Kv1.1, Kv1.2 and Kv1.6 influence excitability of rat visceral sensory neurons. J. Physiol. 2002, 541:467-482.
20. Grissmer S., Nguyen A.N., Aiyar J., Hanson D.C., Mather R.J., Gutman G.A., Karmilowicz M.J., Auperin D.D., Chandy K.G. Pharmacological characterization of five cloned voltage-gated K+ channels, types Kv1.1, 1.2, 1.3, 1.5, and 3.1, stably expressed in mammalian cell lines. Mol. Pharmacol. 1994, 45:1227-1234.
21. Hainsworth R. Reflexes from the heart. Physiol. Rev. 1991, 71:617-658.
22. Hainsworth R., Ledsome J.R., Carswell F. Reflex responses from aortic baroreceptors. Am. J. Physiol. 1970, 218:423-429.
23. Hay M., Kunze D.L. Calcium-activated potassium channels in rat visceral sensory afferents. Brain Res. 1994, 639:333-336.
24. Herzog R.I., Cummins T.R., Waxman S.G. Persistent TTX-resistant Na+ current affects resting potential and response to depolarization in simulated spinal sensory neurons. J. Neurophysiol. 2001, 86:1351-1364.
25. Higashi H. Pharmacological aspects of visceral sensory receptors. Prog. Brain Res. 1986, 67:149-162.
26. Hoesch R.E., Weinreich D., Kao J.P. Localized IP3-evoked Ca2+ release activates a K+ current in primary vagal sensory neurons. J. Neurophysiol. 2004, 91:2344-2352.
27. Ikeda S.R., Schofield G.G., Weight F.F. Na+ and Ca2+ currents of acutely isolated adult rat nodose ganglion cells. J. Neurophysiol. 1986, 55:527-539.
28. Katona P.G., Poitras J.W., Pantelakis N., Jensen E.W., Barnett G.O. Deterministic nature of baroreceptor firing. Am. J. Physiol. 1968, 215:1-7.
29. Kline D.D., Buniel M.C., Glazebrook P., Peng Y.J., Ramirez-Navarro A., Prabhakar N.R., Kunze D.L. Kv1.1 deletion augments the afferent hypoxic chemosensory pathway and respiration. J. Neurosci. 2005, 25:3389-3399.
30. Kline D.D., Hendricks G., Hermann G., Rogers R.C., Kunze D.L. Dopamine inhibits N-type channels in visceral afferents to reduce synaptic transmitter release under normoxic and chronic intermittent hypoxic conditions. J. Neurophysiol. 2009, 101:2270-2278.
31. Kobayashi M., Cheng Z.B., Tanaka K., Nosaka S. Is the aortic depressor nerve involved in arterial chemoreflexes in rats?. J. Auton. Nerv. Syst. 1999, 78:38-48.
32. Krauhs J.M. Structure of rat aortic baroreceptors and their relationship to connective tissue. J. Neurocytol. 1979, 8:401-414.
33. Kunze D.L., Andresen M.C. Arterial baroreceptors: excitation and modulation. Reflex Control of the Circulation 1991, 141-166. CRC Press, Boca Raton. I.H. Zucker, J.P. Gilmore (Eds.).
34. Kwong K., Carr M.J., Gibbard A., Savage T.J., Singh K., Jing J.P., Meeker S., Undem B.J. Voltage-gated sodium channels in nociceptive versus non-nociceptive nodose vagal sensory neurons innervating guinea pig lungs. J. Physiol. 2008, 586:1321-1336.
35. Lambert R.C., McKenna F., Maulet Y., Talley E.M., Bayliss D.A., Cribbs L.L., Lee J.H., Perez-Reyes E., Feltz A. Low-voltage-activated Ca2+ currents are generated by members of the CavT subunit family (alpha1G/H) in rat primary sensory neurons. J. Neurosci. 1998, 18:8605-8613.
36. Lancaster E., Oh E.J., Gover T., Weinreich D. Calcium and calcium-activated currents in vagotomized rat primary vagal afferent neurons. J. Physiol. 2002, 540:543-556.
37. Li B.Y., Schild J.H. Patch clamp electrophysiology in nodose ganglia of adult rat. Neurosci. Methods 2002, 115:157-167.
38. Li Z., Chapleau M.W., Bates J.N., Bielefeldt K., Lee H.C., Abboud F.M. Nitric oxide as an autocrine regulator of sodium currents in baroreceptor neurons. Neuron 1998, 20:1039-1049.
39. Li B.Y., Feng B., Tsu H.Y., Schild J.H. Unmyelinated visceral afferents exhibit frequency dependent action potential broadening while myelinated visceral afferents do not. Neurosci. Lett. 2007, 421:62-66.
40. Li B.Y., Qiao G.F., Feng B., Zhao R.B., Lu Y.J., Schild J.H. Electrophysiological and neuroanatomical evidence of sexual dimorphism in aortic baroreceptor and vagal afferents in rat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 295:R1301-R1310.
41. Li B.Y., Glazebrook P., Kunze D.L., Schild J.H. KCa1.1 channel contributes to cell excitability in unmyelinated but not myelinated rat vagal afferents. Am. J. Physiol. Cell Physiol. 2011, 300:C1393-C1403.
42. Loewy A.D. The central nervous organization of reflex circulatory control. Central Regulation of Automatic Functions 1990, 168-188. Oxford University Press, USA. A.D. Loewy, K.M. Spyer (Eds.).
43. Longhurst J.C. Cardiac receptors: their function in health and disease. Prog. Cardiovasc. Dis. 1984, 27:201-222.
44. Lu Y., Ma X., Sabharwal R., Snitsarev V., Morgan D., Rahmouni K., Drummond H.A., Whiteis C.A., Costa V., Price M., Benson C., Welsh M.J., Chapleau M.W., Abboud F.M. The ion channel ASIC2 is required for baroreceptor and autonomic control of the circulation. Neuron 2009, 64:885-897.
45. Mendelowitz D., Kunze D.L. Characterization of calcium currents in aortic baroreceptor neurons. J. Neurophysiol. 1992, 68:509-517.
46. Mendelowitz D., Yang M., Andresen M.C., Kunze D.L. Localization and retention in vitro of fluorescently labeled aortic baroreceptor terminals on neurons from the nucleus tractus solitarius. Brain Res. 1992, 581:339-343.
47. Mendelowitz D., Reynolds P.J., Andresen M.C. Heterogeneous functional expression of calcium channels at sensory and synaptic regions in nodose neurons. J. Neurophysiol. 1995, 73:872-875.
48. Muroi Y., Ru F., Kollarik M., Canning B.J., Hughes S.A., Walsh S., Sigg M., Carr M.J., Undem B.J. Selective silencing of Na(V)1.7 decreases excitability and conduction in vagal sensory neurons. J. Physiol. 2011, 589:5663-5676.
49. Qiao G.F., Li B.Y., Lu Y.J., Fu Y.L., Schild J.H. 17Beta-estradiol restores excitability of a sexually dimorphic subset of myelinated vagal afferents in ovariectomized rats. Am. J. Physiol. Cell Physiol. 2009, 297:C654-C664.
50. Ramirez A.N., Lee D., Glazebrook P.A., Wible B.A., Kunze D.L. Kv2.1 and Kv2.2 potassium channels: role and distribution in the afferent pathway of the arterial baroreflex. FASEB J. 2005, 19:A1159.
51. Ramirez-Navarro A., Glazebrook P.A., Kane-Sutton M., Padro C., Kline D.D., Kunze D.L. Kv1.3 channels regulate synaptic transmission in the nucleus of solitary tract. J. Neurophysiol. 2011, 105:2772-2780.
52. Sapru H.N., Gonzalez E., Krieger A.J. Aortic nerve stimulation in the rat: cardiovascular and respiratory responses. Brain Res. Bull. 1981, 6:393-398.
53. Schild J.H., Kunze D.L. Experimental and modeling study of Na+ current heterogeneity in rat nodose neurons and its impact on neuronal discharge. J. Neurophysiol. 1997, 78:3198-3209.
54. Schild J.H., Clark J.W., Hay M., Mendelowitz D., Andresen M.C., Kunze D.L. A- and C-type rat nodose sensory neurons: model interpretations of dynamic discharge characteristics. J. Neurophysiol. 1994, 71:2338-2358.
55. Schild J.H., Alfrey K.D., Li B.Y. Voltage-gated ion channels in vagal afferent neurons. Advances in Vagal Afferent Neurobiology 2005, 77-100. CRC Press, USA. B.J. Undem, D. Weinreich (Eds.).
56. Sharman J.L., Mpamhanga C.P., Spedding M., Germain P., Staels B., Dacquet C., Laudet V., Harmar A.J., NC-IUPHAR IUPHAR-DB: new receptors and tools for easy searching and visualization of pharmacological data. Nucl. Acids Res. 2011, 39:D534-D538.
57. Stansfeld C.E., Wallis D.I. Properties of visceral primary afferent neurons in the nodose ganglion of the rabbit. J. Neurophysiol. 1985, 54:245-260.
58. Tatalovic M., Glazebrook P.A., Kunze D.L. Expression of the P/Q (Cav2.1) calcium channel in nodose sensory neurons and arterial baroreceptors. Neurosci. Lett. 2012, 520:38-42.
59. Thoren P., Jones J.V. Characteristics of aortic baroreceptor C-fibres in the rabbit. Acta Physiol. Scand. 1977, 99:448-456.
60. Thorén P., Saum W.R., Brown A.M. Characteristics of rat aortic baroreceptors with nonmedullated afferent nerve fibers. Circ. Res. 1977, 40:231-237.
61. Tu H., Zhang L., Tran T.P., Muelleman R.L., Li Y.L. Reduced expression and activation of voltage-gated sodium channels contributes to blunted baroreflex sensitivity in heart failure rats. J. Neurosci. Res. 2010, 88:3337-3349.
62. Tu H., Liu J., Zhu Z., Zhang L., Pipinos I.I., Li Y.L. Mitochondria-derived superoxide and voltage-gated sodium channels in baroreceptor neurons from chronic heart-failure rats. J. Neurophysiol. 2012, 107:591-602.
63. Undem B.J., Weinreich D. Electrophysiological properties and chemosensitivity of guinea pig nodose ganglion neurons in vitro. Auton. Nerv. Syst. 1993, 44:17-33.
64. Viscomi C., Altomare C., Bucchi A., Camatini E., Baruscotti M., Moroni A., DiFrancesco D. C terminus-mediated control of voltage and cAMP gating of hyperpolarization-activated cyclic nucleotide-gated channels. J. Biol. Chem. 2001, 276:29930-29934.
65. Wainger B.J., DeGennaro M., Santoro B., Siegelbaum S.A., Tibbs G.R. Molecular mechanism of cAMP modulation of HCN pacemaker channels. Nature 2001, 411:805-810.
66. Wang J., Chen S., Siegelbaum S.A. Regulation of hyperpolarization-activated HCN channel gating and cAMP modulation due to interactions of COOH terminus and core transmembrane regions. J. Gen. Physiol. 2001, 118:237-250.
67. Wladyka C.L., Kunze D.L. KCNQ/M-currents contribute to the resting membrane potential in rat visceral sensory neurons. J. Physiol. 2006, 575:175-189.
68. Wladyka C.L., Feng B., Glazebrook P.A., Schild J.H., Kunze D.L. The KCNQ/M-current modulates arterial baroreceptor function at the sensory terminal in rats. J. Physiol. 2008, 586:795-802.
69. Zhou Y.H., Sun L.H., Liu Z.H., Bu G., Pang X.P., Sun S.C., Qiao G.F., Li B.Y., Schild J.H. Functional impact of the hyperpolarization-activated current on the excitability of myelinated A-type vagal afferent neurons in the rat. Clin. Exp. Pharmacol. Physiol. 2010, 37:852-861.