Secondhand smoke exposure alters K+ channel function and intrinsic cell excitability in a subset of second-order airway neurons in the nucleus tractus solitarius of young guinea pigs

European Journal of Neuroscience

Volumn 31, Issue 4, 2010, Pages 673-684

  Sekizawa, Shin Ichi ^a   Joad, Jesse P ^a   Pinkerton, Kent E ^b   Bonham, Ann C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Airway afferent fibers; Environmental air pollutants; Intrinsic cell excitability; Ion channels; K+ currents; Postsynaptic neurons

Indexed keywords

4 AMINOPYRIDINE; POTASSIUM CHANNEL; TETRYLAMMONIUM;

ACTION POTENTIAL; AFTERHYPERPOLARIZATION; AIRWAY; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN SLICE; BRAIN STEM; CELL MEMBRANE DEPOLARIZATION; CHILDHOOD; CONTROLLED STUDY; ELECTRIC CURRENT; ENVIRONMENTAL EXPOSURE; GUINEA PIG; HERING BREUER REFLEX; LUNG; MALE; NERVE CELL; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; NONHUMAN; PASSIVE SMOKING; PATCH CLAMP; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; SENSORY NERVE CELL; SOLITARY TRACT NUCLEUS; SPIKE WAVE; STEADY STATE; WHOLE CELL;

4-AMINOPYRIDINE; ACTION POTENTIALS; ANIMALS; GUINEA PIGS; LUNG; MALE; MEMBRANE POTENTIALS; NEUROANATOMICAL TRACT-TRACING TECHNIQUES; NEURONS, AFFERENT; POTASSIUM CHANNEL BLOCKERS; RANDOM ALLOCATION; SOLITARY NUCLEUS; TETRAETHYLAMMONIUM; TOBACCO SMOKE POLLUTION;

EID: 76949091365     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07093.x     Document Type: Article

References (57)

1. Annesi-Maesano, I., Agabiti, N., Pistelli, R., Couilliot, M.F. Forastiere, F. (2003) Subpopulations at increased risk of adverse health outcomes from air pollution. Eur. Respir. J. Suppl., 40, 57s 63s.
2. Bailey, T.W., Jin, Y.H., Doyle, M.W. Andresen, M.C. (2002) Vanilloid-sensitive afferents activate neurons with prominent A-type potassium currents in nucleus tractus solitarius. J. Neurosci., 22, 8230 8237.
3. Baines, R.A., Uhler, J.P., Thompson, A., Sweeney, S.T. Bate, M. (2001) Altered electrical properties in Drosophila neurons developing without synaptic transmission. J. Neurosci., 21, 1523 1531.
4. Belugin, S. Mifflin, S. (2005) Transient voltage-dependent potassium currents are reduced in NTS neurons isolated from renal wrap hypertensive rats. J. Neurophysiol., 94, 3849 3859.
5. Bonham, A.C. Joad, J.P. (1991) Neurones in commissural nucleus tractus solitarii required for full expression of the pulmonary C fibre reflex in rat. J. Physiol., 441, 95 112.
6. Bonham, A.C. McCrimmon, D.R. (1990) Neurones in a discrete region of the nucleus tractus solitarius are required for the Breuer-Hering reflex in rat. J. Physiol., 427, 261 280.
7. Bonham, A.C., Kappagoda, C.T., Kott, K.S. Joad, J.P. (1995) Exposing young guinea pigs to sidestream tobacco smoke decreases rapidly adapting receptor responsiveness. J. Appl. Physiol., 78, 1412 1420.
8. + channel expression distinguishes subpopulations of parvalbumin- and somatostatin-containing neocortical interneurons. J. Neurosci., 19, 9332 9345.
9. Cunningham, J., O'Connor, G.T., Dockery, D.W. Speizer, F.E. (1996) Environmental tobacco smoke, wheezing, and asthma in children in 24 communities. Am. J. Respir. Crit. Care Med., 153, 218 224.
10. Dallas, M.L., Atkinson, L., Milligan, C.J., Morris, N.P., Lewis, D.I., Deuchars, S.A. Deuchars, J. (2005) Localization and function of the Kv3.1b subunit in the rat medulla oblongata: focus on the nucleus tractus solitarii. J. Physiol., 562, 655 672.
11. Dekin, M.S., Getting, P.A. Johnson, S.M. (1987) In vitro characterization of neurons in the ventral part of the nucleus tractus solitarius. I. Identification of neuronal types and repetitive firing properties. J. Neurophysiol., 58, 195 214.
12. Desai, N.S., Rutherford, L.C. Turrigiano, G.G. (1999) Plasticity in the intrinsic excitability of cortical pyramidal neurons. Nat. Neurosci., 2, 515 520.
13. Deuchars, S.A., Brooke, R.E., Frater, B. Deuchars, J. (2001) Properties of interneurones in the intermediolateral cell column of the rat spinal cord: role of the potassium channel subunit Kv3.1. Neuroscience, 106, 433 446.
14. Dodge, R. (1982) The effects of indoor pollution on Arizona children. Arch. Environ. Health, 37, 151 155.
15. Du, J., Zhang, L., Weiser, M., Rudy, B. McBain, C.J. (1996) Developmental expression and functional characterization of the potassium-channel subunit Kv3.1b in parvalbumin-containing interneurons of the rat hippocampus. J. Neurosci., 16, 506 518.
16. Ekwo, E.E., Weinberger, M.M., Lachenbruch, P.A. Huntley, W.H. (1983) Relationship of parental smoking and gas cooking to respiratory disease in children. Chest, 84, 662 668.
17. Frick, A., Magee, J. Johnston, D. (2004) LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites. Nat. Neurosci., 7, 126 135.
18. Fu, Y. Neugebauer, V. (2008) Differential mechanisms of CRF1 and CRF2 receptor functions in the amygdala in pain-related synaptic facilitation and behavior. J. Neurosci., 28, 3861 3876.
19. Gibson, P.G., Simpson, J.L., Chalmers, A.C., Toneguzzi, R.C., Wark, P.A., Wilson, A.J. Hensley, M.J. (2001) Airway eosinophilia is associated with wheeze but is uncommon in children with persistent cough and frequent chest colds. Am. J. Respir. Crit. Care Med., 164, 977 981.
20. Gross, P.M., Wall, K.M., Pang, J.J., Shaver, S.W. Wainman, D.S. (1990) Microvascular specializations promoting rapid interstitial solute dispersion in nucleus tractus solitarius. Am. J. Physiol., 259, R1131 R1138.
21. Hsiao, C.F., Gougar, K., Asai, J. Chandler, S.H. (2007) Intrinsic membrane properties and morphological characteristics of interneurons in the rat supratrigeminal region. J. Neurosci. Res., 85, 3673 3686.
22. Joad, J.P., Munch, P.A., Bric, J.M., Evans, S.J., Pinkerton, K.E., Chen, C.Y. Bonham, A.C. (2004) Passive smoke effects on cough and airways in young guinea pigs: role of brainstem substance P. Am. J. Respir. Crit. Care Med., 169, 499 504.
23. Kim, J., Wei, D.S. Hoffman, D.A. (2005) Kv4 potassium channel subunits control action potential repolarization and frequency-dependent broadening in rat hippocampal CA1 pyramidal neurones. J. Physiol., 569, 41 57.
24. + channels during synaptically driven action potentials in the MNTB. J. Neurophysiol., 96, 1547 1555.
25. van der Kooy, D. Koda, L.Y. (1983) Organization of the projections of a circumventricular organ: the area postrema in the rat. J. Comp. Neurol., 219, 328 338.
26. Li, C.Y., Lu, J.T., Wu, C.P., Duan, S.M. Poo, M.M. (2004) Bidirectional modification of presynaptic neuronal excitability accompanying spike timing-dependent synaptic plasticity. Neuron, 41, 257 268.
27. Massengill, J.L., Smith, M.A., Son, D.I. O'Dowd, D.K. (1997) Differential expression of K4-AP currents and Kv3.1 potassium channel transcripts in cortical neurons that develop distinct firing phenotypes. J. Neurosci., 17, 3136 3147.
28. Miura, A., Kawatani, M., Araki, I. de Groat, W.C. (2000) Electrophysiological properties of lumbosacral preganglionic neurons in the neonatal rat spinal cord. Brain Res., 872, 54 63.
29. Miyazaki, M., Arata, A., Tanaka, I. Ezure, K. (1998) Activity of rat pump neurons is modulated with central respiratory rhythm. Neurosci. Lett., 249, 61 64.
30. Moak, J.P. Kunze, D.L. (1993) Potassium currents of neurons isolated from medial nucleus tractus solitarius. Am. J. Physiol., 265, H1596 H1602.
31. Mutoh, T., Bonham, A.C., Kott, K.S. Joad, J.P. (1999) Chronic exposure to sidestream tobacco smoke augments lung C-fiber responsiveness in young guinea pigs. J. Appl. Physiol., 87, 757 768.
32. Nakajima, S. Onodera, K. (1969) Membrane properties of the stretch receptor neurones of crayfish with particular reference to mechanisms of sensory adaptation. J. Physiol., 200, 161 185.
33. Paton, J.F. (1998) Convergence properties of solitary tract neurones driven synaptically by cardiac vagal afferents in the mouse. J. Physiol., 508, 237 252.
34. Paton, J.F., Foster, W.R. Schwaber, J.S. (1993) Characteristic firing behavior of cell types in the cardiorespiratory region of the nucleus tractus solitarii of the rat. Brain Res., 604, 112 125.
35. Perney, T.M. Kaczmarek, L.K. (1997) Localization of a high threshold potassium channel in the rat cochlear nucleus. J. Comp. Neurol., 386, 178 202.
36. Perney, T.M., Marshall, J., Martin, K.A., Hockfield, S. Kaczmarek, L.K. (1992) Expression of the mRNAs for the Kv3.1 potassium channel gene in the adult and developing rat brain. J. Neurophysiol., 68, 756 766.
37. Rudy, B. (1988) Diversity and ubiquity of K channels. Neuroscience, 25, 729 749.
38. + channels designed for high-frequency repetitive firing. Trends Neurosci., 24, 517 526.
39. Rudy, B., Kentros, C., Weiser, M., Fruhling, D., Serodio, P., Vega-Saenz de Miera, E., Ellisman, M.H., Pollock, J.A. Baker, H. (1992) Region-specific expression of a K+ channel gene in brain. Proc. Natl Acad. Sci. USA, 89, 4603 4607.
40. Rudy, B., Chow, A., Lau, D., Amarillo, Y., Ozaita, A., Saganich, M., Moreno, H., Nadal, M.S., Hernandez-Pineda, R., Hernandez-Cruz, A., Erisir, A., Leonard, C. Vega-Saenz de, M.E. (1999) Contributions of Kv3 channels to neuronal excitability. Ann. NY Acad. Sci., 868, 304 343.
41. Sanchez-Andres, J.V. Alkon, D.L. (1991) Voltage-clamp analysis of the effects of classical conditioning on the hippocampus. J. Neurophysiol., 65, 796 807.
42. Sant'Ambrogio, G. (1982) Information arising from the tracheobronchial tree of mammals. Physiol. Rev., 62, 531 569.
43. 2+ exchange current. J. Neurophysiol., 95, 882 892.
44. Sekizawa, S.I., French, A.S., Hoger, U. Torkkeli, P.H. (1999) Voltage-activated potassium outward currents in two types of spider mechanoreceptor neurons. J. Neurophysiol., 81, 2937 2944.
45. Sekizawa, S., Joad, J.P. Bonham, A.C. (2003) Substance P presynaptically depresses the transmission of sensory input to bronchopulmonary neurons in the guinea pig nucleus tractus solitarii. J. Physiol., 552, 547 559.
46. Sekizawa, S., Chen, C.Y., Bechtold, A.G., Tabor, J.M., Bric, J.M., Pinkerton, K.E., Joad, J.P. Bonham, A.C. (2008) Extended secondhand tobacco smoke exposure induces plasticity in nucleus tractus solitarius second-order lung afferent neurons in young guinea pigs. Eur. J. Neurosci., 28, 771 781.
47. Sekizawa, S., Bechtold, A.G., Tham, R.C. Bonham, A.C. (2009) A novel postsynaptic group II metabotropic glutamate receptor role in modulating baroreceptor signal transmission. J. Neurosci., 29, 11807 11816.
48. Sekizawa, S., Joad, J.P., Pinkerton, K.E. Bonham, A.C. (2010) Secondhand tobacco smoke exposure differentially alters nucleus tractus solitarius neurons at two different ages in developing non-human primates. Toxicol. Appl. Pharmacol., 242, 199 208.
49. Sonner, P.M. Stern, J.E. (2007) Functional role of A-type potassium currents in rat presympathetic PVN neurones. J. Physiol., 582, 1219 1238.
50. Tell, F. Bradley, R.M. (1994) Whole-cell analysis of ionic currents underlying the firing pattern of neurons in the gustatory zone of the nucleus tractus solitarii. J. Neurophysiol., 71, 479 492.
51. Turrigiano, G., LeMasson, G. Marder, E. (1995) Selective regulation of current densities underlies spontaneous changes in the activity of cultured neurons. J. Neurosci., 15, 3640 3652.
52. + currents influence firing properties of isolectin B4-positive but not isolectin B4-negative primary sensory neurons. J. Neurophysiol., 93, 3401 3409.
53. Wallach, J.H. Loewy, A.D. (1980) Projections of the aortic nerve to the nucleus tractus solitarius in the rabbit. Brain Res., 188, 247 251.
54. Wang, X., Wypij, D., Gold, D.R., Speizer, F.E., Ware, J.H., Ferris, B.G. Jr. Dockery, D.W. (1994) A longitudinal study of the effects of parental smoking on pulmonary function in children 6-18 years. Am. J. Respir. Crit. Care Med., 149, 1420 1425.
55. Weiser, M., Bueno, E., Sekirnjak, C., Martone, M.E., Baker, H., Hillman, D., Chen, S., Thornhill, W., Ellisman, M. Rudy, B. (1995) The potassium channel subunit KV3.1b is localized to somatic and axonal membranes of specific populations of CNS neurons. J. Neurosci., 15, 4298 4314.
56. Weitzman, M., Gortmaker, S., Walker, D.K. Sobol, A. (1990) Maternal smoking and childhood asthma. Pediatrics, 85, 505 511.
57. Zhou, F.M. Hablitz, J.J. (1996) Layer I neurons of rat neocortex. I. Action potential and repetitive firing properties. J. Neurophysiol., 76, 651 667.