Secondhand tobacco smoke exposure differentially alters nucleus tractus solitarius neurons at two different ages in developing non-human primates

Toxicology and Applied Pharmacology

Volumn 242, Issue 2, 2010, Pages 199-208

  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 sensory afferents; Indoor air pollutant; Infant; Intrinsic cell excitability; Nucleus tractus solitarius; Primates; Respiration; Secondhand smoke; Synaptic transmission

Indexed keywords

TOBACCO SMOKE;

AGE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTHMA; BRONCHIOLITIS; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; GESTATIONAL AGE; LONG TERM EXPOSURE; LUNG FUNCTION; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NERVE POTENTIAL; NERVOUS SYSTEM DEVELOPMENT; NEUROMODULATION; NONHUMAN; PASSIVE SMOKING; PERINATAL PERIOD; PHENOTYPE; RHESUS MONKEY; RISK ASSESSMENT; SOLITARY TRACT NUCLEUS; SUDDEN INFANT DEATH SYNDROME; SYNAPTIC TRANSMISSION; TOXICITY TESTING;

ANIMALS; FEMALE; MACACA MULATTA; NEURONS; PATCH-CLAMP TECHNIQUES; PREGNANCY; SOLITARY NUCLEUS; TOBACCO SMOKE POLLUTION;

ANIMALIA; MACACA MULATTA; NICOTIANA TABACUM; PRIMATES;

EID: 71049123173     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2009.10.009     Document Type: Article

References (47)

1. Anderson R.L., Jobling P., and Gibbins I.L. Development of electrophysiological and morphological diversity in autonomic neurons. J. Neurophysiol. 86 (2001) 1237-1251
2. Annesi-Maesano I., Agabiti N., Pistelli R., Couilliot M.F., and Forastiere F. Subpopulations at increased risk of adverse health outcomes from air pollution. Eur. Respir. J. Suppl. 40 (2003) 57s-63s
3. Bailey T.W., Jin Y.H., Doyle M.W., and Andresen M.C. Vanilloid-sensitive afferents activate neurons with prominent A-type potassium currents in nucleus tractus solitarius. J. Neurosci. 22 (2002) 8230-8237
4. Bland M., Bewley B.R., Pollard V., and Banks M.H. Effect of children's and parents' smoking on respiratory symptoms. Arch. Dis. Child. 53 (1978) 100-105
5. Bouzigon E., Corda E., Aschard H., Dizier M.H., Boland A., Bousquet J., Chateigner N., Gormand F., Just J., Le M.N., Scheinmann P., Siroux V., Vervloet D., Zelenika D., Pin I., Kauffmann F., Lathrop M., and Demenais F. Effect of 17q21 variants and smoking exposure in early-onset asthma. N. Engl. J. Med. 359 (2008) 1985-1994
6. Cameron J.S., and Dryer S.E. BK-Type K(Ca) channels in two parasympathetic cell types: differences in kinetic properties and developmental expression. J. Neurophysiol. 84 (2000) 2767-2776
7. Chen C.Y., Horowitz J.M., and Bonham A.C. A presynaptic mechanism contributes to depression of autonomic signal transmission in NTS. Am. J. Physiol. 277 (1999) H1350-H1360
8. Coleridge J.C., and Coleridge H.M. Afferent vagal C fibre innervation of the lungs and airways and its functional significance. Rev. Physiol. Biochem. Pharmacol. 99 (1984) 1-110
9. Coleridge H.M., Coleridge J.C., and Schultz H.D. Afferent pathways involved in reflex regulation of airway smooth muscle. Pharmacol. Ther. 42 (1989) 1-63
10. Connor J.A., and Stevens C.F. Prediction of repetitive firing behaviour from voltage clamp data on an isolated neurone soma. J. Physiol. 213 (1971) 31-53
11. Cunningham J., O'Connor G.T., Dockery D.W., and Speizer F.E. Environmental tobacco smoke, wheezing, and asthma in children in 24 communities. Am. J. Respir. Crit. Care Med. 153 (1996) 218-224
12. Dekin M.S., Getting P.A., and Johnson S.M. 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 (1987) 195-214
13. DiFranza J.R., and Lew R.A. Effect of maternal cigarette smoking on pregnancy complications and sudden infant death syndrome. J. Fam. Pract. 40 (1995) 385-394
14. Durand G.M., Kovalchuk Y., and Konnerth A. Long-term potentiation and functional synapse induction in developing hippocampus. Nature 381 (1996) 71-75
15. Fleming P., and Blair P.S. Sudden infant death syndrome and parental smoking. Early Hum. Dev. 83 (2007) 721-725
16. Franks K.M., and Isaacson J.S. Synapse-specific downregulation of NMDA receptors by early experience: a critical period for plasticity of sensory input to olfactory cortex. Neuron 47 (2005) 101-114
17. Gibson P.G., Simpson J.L., Chalmers A.C., Toneguzzi R.C., Wark P.A., Wilson A.J., and Hensley M.J. 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 (2001) 977-981
18. Golub M.S., and Gershwin M.E. Standardized neonatal assessment in the rhesus monkey. In: Anonymous N.P., and Parer J. (Eds). Research in perinatal medicine (1). (1984), Perinatology Press, Ithaca, NY 56-87
19. Gonzalez-Burgos G., Kroener S., Zaitsev A.V., Povysheva N.V., Krimer L.S., Barrionuevo G., and Lewis D.A. Functional maturation of excitatory synapses in layer 3 pyramidal neurons during postnatal development of the primate prefrontal cortex. Cereb. Cortex 18 (2008) 626-637
20. Joad J.P., Kott K.S., Bric J.M., Peake J.L., Plopper C.G., Schelegle E.S., Gershwin L.J., and Pinkerton K.E. Structural and functional localization of airway effects from episodic exposure of infant monkeys to allergen and/or ozone. Toxicol. Appl. Pharmacol. 214 (2006) 237-243
21. Kim J., Wei D.S., and Hoffman D.A. Kv4 potassium channel subunits control action potential repolarization and frequency-dependent broadening in rat hippocampal CA1 pyramidal neurones. J. Physiol. 569 (2005) 41-57
22. Kline D.D., Takacs K.N., Ficker E., and Kunze D.L. Dopamine modulates synaptic transmission in the nucleus of the solitary tract. J. Neurophysiol. 88 (2002) 2736-2744
23. Kubin L., Alheid G.F., Zuperku E.J., and McCrimmon D.R. Central pathways of pulmonary and lower airway vagal afferents. J. Appl. Physiol. 101 (2006) 618-627
24. Lee L.Y., and Pisarri T.E. Afferent properties and reflex functions of bronchopulmonary C-fibers. Respir. Physiol. 125 (2001) 47-65
25. Liao D., Zhang X., O'Brien R., Ehlers M.D., and Huganir R.L. Regulation of morphological postsynaptic silent synapses in developing hippocampal neurons. Nat. Neurosci. 2 (1999) 37-43
26. Machaalani R., and Waters K.A. Neuronal cell death in the sudden infant death syndrome brainstem and associations with risk factors. Brain 131 (2008) 218-228
27. Matturri L., Ottaviani G., and Lavezzi A.M. Maternal smoking and sudden infant death syndrome: epidemiological study related to pathology. Virchows Arch. 449 (2006) 697-706
28. Miles R. Frequency dependence of synaptic transmission in nucleus of the solitary tract in vitro. J. Neurophysiol. 55 (1986) 1076-1090
29. Morgan W.J., Stern D.A., Sherrill D.L., Guerra S., Holberg C.J., Guilbert T.W., Taussig L.M., Wright A.L., and Martinez F.D. Outcome of asthma and wheezing in the first 6 years of life: follow-up through adolescence. Am. J. Respir. Crit. Care Med. 172 (2005) 1253-1258
30. Nakajima S., and Onodera K. Membrane properties of the stretch receptor neurones of crayfish with particular reference to mechanisms of sensory adaptation. J. Physiol. 200 (1969) 161-185
31. Paton J.F., Foster W.R., and Schwaber J.S. Characteristic firing behavior of cell types in the cardiorespiratory region of the nucleus tractus solitarii of the rat. Brain Res. 604 (1993) 112-125
32. Plopper C.G., and Hyde D.M. The non-human primate as a model for studying COPD and asthma. Pulm. Pharmacol. Ther. 21 (2008) 755-766
33. Pollack H.A. Sudden infant death syndrome, maternal smoking during pregnancy, and the cost-effectiveness of smoking cessation intervention. Am. J. Public Health 91 (2001) 432-436
34. Rogawski M.A. The A-current: how ubiquitous a feature of excitable cells is it?. Trends Neurosci. 8 (1985) 214-219
35. Rudy B. Diversity and ubiquity of K channels. Neuroscience 25 (1988) 729-749
36. 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., and Vega-Saenz de M.E. Contributions of Kv3 channels to neuronal excitability. Ann. N Y. Acad. Sci. 868 (1999) 304-343
37. Sant'Ambrogio G., and Widdicombe J. Reflexes from airway rapidly adapting receptors. Respir. Physiol. 125 (2001) 33-45
38. Saporta S., Willing A.E., Colina L.O., Zigova T., Milliken M., Daadi M.M., and Sanberg P.R. In vitro and in vivo characterization of hNT neuron neurotransmitter phenotypes. Brain Res. Bull. 53 (2000) 263-268
39. Scheuer D.A., Zhang J., Toney G.M., and Mifflin S.W. Temporal processing of aortic nerve evoked activity in the nucleus of the solitary tract. J. Neurophysiol. 76 (1996) 3750-3757
40. Sekizawa S., Joad J.P., and Bonham A.C. Substance P presynaptically depresses the transmission of sensory input to bronchopulmonary neurons in the guinea pig nucleus tractus solitarii. J. Physiol. 552 (2003) 547-559
41. Serodio P., and Rudy B. Differential expression of Kv4 K+ channel subunits mediating subthreshold transient K+ (A-type) currents in rat brain. J. Neurophysiol. 79 (1998) 1081-1091
42. Wang X., Wypij D., Gold D.R., Speizer F.E., Ware J.H., Ferris Jr. B.G., and Dockery D.W. A longitudinal study of the effects of parental smoking on pulmonary function in children 6-18 years. Am. J. Respir. Crit. Care Med. 149 (1994) 1420-1425
43. Weitzman M., Gortmaker S., Walker D.K., and Sobol A. Maternal smoking and childhood asthma. Pediatrics 85 (1990) 505-511
44. Widdicombe J., and Lee L.Y. Airway reflexes, autonomic function, and cardiovascular responses. Environ. Health Perspect. 109 Suppl 4 (2001) 579-584
45. Wisborg K., Kesmodel U., Henriksen T.B., Olsen S.F., and Secher N.J. A prospective study of smoking during pregnancy and SIDS. Arch. Dis. Child 83 (2000) 203-206
46. Wu G., Malinow R., and Cline H.T. Maturation of a central glutamatergic synapse. Science 274 (1996) 972-976
47. Yunginger J.W., Reed C.E., O'Connell E.J., Melton III L.J., O'Fallon W.M., and Silverstein M.D. A community-based study of the epidemiology of asthma. Incidence rates, 1964-1983. Am. Rev. Respir. Dis. 146 (1992) 888-894