Prenatal nicotine increases pulmonary α7 nicotinic receptor expression and alters fetal lung development in monkeys

Journal of Clinical Investigation

Volumn 103, Issue 5, 1999, Pages 637-647

  Sekhon, Harmanjatinder S ^a   Yibing, Jia ^a   Raab, Renee ^a   Kuryatov, Alexander ^b   Pankow, James F ^c   Whitsett, Jeffrey A ^d   Lindstrom, Jon ^b   Spindel, Eliot R ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTINE; NICOTINIC RECEPTOR;

ARTICLE; BLOOD PLACENTA BARRIER; CELL SPECIFICITY; FEMALE; GENE EXPRESSION; HISTOPATHOLOGY; IMMUNOCYTOCHEMISTRY; LOW BIRTH WEIGHT; LUNG DEVELOPMENT; LUNG FUNCTION; LUNG HYPOPLASIA; MONKEY; NONHUMAN; PREMATURITY; PRENATAL EXPOSURE; PRIORITY JOURNAL; RECEPTOR BINDING; RESPIRATORY TRACT DISEASE; SMOKING;

EID: 0344958586     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI5232     Document Type: Article

References (55)

1. Cliver, S.P., et al. 1995. The effect of cigarette smoking on neonatal anthropometric measurements. Obstet. Gynecol. 85:625-630.
2. Kramer, M.S. 1987. Intrauterine growth and gestational duration determinants. Pediatrics. 80:502-511.
3. Taylor, B., and Wadswotth, J. 1987. Maternal smoking during pregnancy and lower respiratory tract illness in early life. Arch. Dis. Child. 62:786-791.
4. Tager, I. B., et al. 1992. Lung function, pre- and post-natal smoke exposure, and wheezing in the first year of life. Am. Rev. Respir. Dis. 147:811-817.
5. Hanrahan, J., et al. 1992. The effect of maternal smoking during pregnancy on early infant lung function. Am. Rev. Respir. Dis. 145:1129-1135.
6. Cunningham, J., Dockery, D.W., and Speizer, F.E. 1994. Maternal smoking during pregnancy as a predictor of lung function in children. Am. J. Epidemiol. 139:1139-1152.
7. Stoddard, J.J., and Gray, B. 1997. Maternal smoking and medical expenditures for childhood respiratory illness. Am. J. Public Health. 87:205-208.
8. Collins, M.H., et al. 1985. Fetal lung hypoplasia associated with maternal smoking: a morphometric analysis. Pediatr. Res. 19:408-412.
9. Maritz, G.S., Woolward, K.M., and du Toit, G. 1993. Maternal nicotine exposure during pregnancy and development of emphysema-like damage in the offspring. S. Afr. Med. J. 83:195-198.
10. Maritz, G.S., and Thomas, R.A. 1995. Maternal nicotine exposure: response of type II pneumocytes of neonatal rat pups. Cell Biol. Int. 19:323-331.
11. Thurlbeck, W.M. 1995. Lung growth and development. In Pathology of the lung. W.M. Thurlbeck and A.M. Churg, editors. Thieme Medical Publishers. New York, NY. 37-88.
12. Lindstrom, J., et al. 1996. Structure and function of neuronal nicotinic acetylcholine receptors. Prog. Brain Res. 109:125-37.
13. Peng, X., Gerzanich, V., Anand, R., Wang, F., and Lindstrom, J. 1997. Chronic nicotine treatment up-regulates α3 and α7 acetylcholine receptor subtypes expressed by the human neuroblastoma cell line SH-SY5Y. Mol. Pharmacol. 51:776-784.
14. 3H]nicotine binding in human postmortem brain. J. Pharmacol. Exp. Ther. 282:7-13.
15. Marks, M.J., et al. 1992. Nicotine binding and nicotinic receptor subunit RNA after chronic nicotine treatment. J. Neurosci. 12:2765-2784.
16. van de Kamp, J.L., and Collins, A.C. 1994. Prenatal nicotine alters nicotinic receptor development in the mouse brain. Pharmacol. Biochem. Behav. 47:889-900.
17. 3H]nicotine binding sites in brain regions of rats exposed to nicotine prenatally via maternal injections or infusions. J. Pharmacol. Exp. Ther. 242:232-237.
18. Zia, S., Ndoye, A., Nguyen, V.T., and Grando, S.A. 1997. Nicotine enhances expression of the alpha 3, alpha 4, alpha 5, and alpha 7 nicotinic receptors modulating calcium metabolism and regulating adhesion and motility of respiratory epithelial cells. Res. Commun. Mol. Pathol. Pharmacol. 97:243-262.
19. Maus, A.D.J., et al. 1998. Human and rodent bronchial epithelial cells express functional nicotinic acetylcholine receptors. Mol. Pharmacol. 54:779-788.
20. Quik, M., Chan, J., and Patrick, J. 1994. alpha-Bungarotoxin blocks the nicotinic receptor mediated increase in cell number in a neuroendocrine cell line. Brain Res. 655:161-167.
21. Pau, K.Y., Berna, M., Hess, D.L., and Spies, H.G. 1993. Preovulatory gonadotropin-releasing hormone surge in ovarian-intact rhesus macaques. Endocrinology. 133:1650-1656.
22. Scherle, W. 1970. Simple method for volumetry of organs in quantitative stereology. Mikroskopie. 26:57-60.
23. Weibel, E.R. 1979. Stereological methods. Practical methods for biological morphometry, Volume 1. Academic Press. London, United Kingdom. 1-179.
24. Ten Have-Opbroek, A.A.W. 1981. The development of the lung in mammals: an analysis of concepts and findings. Am. J. Anat. 162:201-219.
25. Ten Have-Opbroek, A.A., and Plopper, C.G. 1992. Morphogenetic and functional activity of type II cells in early fetal rhesus monkey lungs. A comparison between primates and rodents. Anat. Rec. 234:93-104.
26. Lindstrom, J. 1996. Neuronal nicotinic acetylcholine receptors. In Ion channels. T. Narahashi, editor. Plenum Press. New York, NY. 377-450.
27. Schoepfer, R., Conroy, W.G., Whiting, P., Gore, M., and Lindstrom, J. 1990. Brain alpha-bungarotoxin binding protein cDNAs and MAbs reveal sub types of this branch of the ligand-gated ion channel gene superfamily. Neuron. 5:35-48.
28. Peng, X., Katz, M., Gerzanich, V., Anand, R., and Lindstrom, J. 1994. Human alpha 7 acetylcholine receptor: cloning of the alpha 7 subunit from the SH-SY5Y cell line and determination of pharmacological properties of native receptors and functional alpha 7 homomers expressed in Xenopus oocytes. Mol. Pharmacol. 45:546-554.
29. Pankow, J.F., et al. 1997. Conversion of nicotine in tobacco smoke to its volatile and available free-base form through the action of gaseous ammonia. Environ. Sci. Technol. 31:2428-2433.
30. Li, K., Nagalla, S.R., and Spindel, E.R. 1994. A rhesus monkey model to characterize the role of gastrin-releasing peptide (GRP) in lung development. Evidence for stimulation of airway growth. J. Clin. Invest. 94:1605-1615.
31. Li, C., Chen, P., and Smith, M.S. 1998. The acute suckling stimulus induces expression of neuropeptide Y (NPY) in cells in the dorsomedial hypothalamus and increases NPY expression in the arcuate nucleus. Endocrinology. 139:1645-1652.
32. Breese, C.R., et al. 1997. Comparison of the regional expression of nicotinic acetylcholine receptor alpha7 mRNA and [125I]-alpha-bungarotoxin binding in human postmortem brain. J. Comp. Neurol. 387:385-398.
33. Plopper, C.G., et al. 1992. Acceleration of alveolar type II cell differentiation in fetal rhesus monkey lung by administration of EGF. Am. J. Physiol. 262:L313-L321.
34. Pryhuber, G.S., Hull, W.M., Fink, I., McMahan, M.J., and Whitsett, J.A. 1991. Ontogeny of surfactant proteins A and Bin human amniotic fluid as indices of fetal lung maturity. Pediatr. Res. 30:597-605.
35. Luck, W., Nau, H., Hansen, R., and Steldinger, R. 1985. Extent of nicotine and cotinine transfer to the human fetus, placenta and amniotic fluid of smoking mothers. Dev. Pharmacol. Ther. 8:384-395.
36. Wang, F., et al. 1996. Assembly of human neuronal nicotinic receptor alpha5 subunits with alpha3, beta2, and beta4 subunits. J. Biol. Chem. 271:17656-17665.
37. Elliot, J., Vullermin, P., and Robinson, P. 1998. Maternal cigarette smoking is associated with increased inner airway wall thickness in children who die from sudden infant death syndrome. Am. J. Respir. Crit. Care Med. 158:802-806.
38. Chen, M.F., Kimizuka, G., and Wang, N.S. 1987. Human fetal lung changes associated with maternal smoking during pregnancy. Pediatr. Pulmonol. 3:51-58.
39. Keith, I.M., and Cary, J.R. 1988. Maternal smoking during pregnancy affects neuroendocrine cells in the neonate hamster lung. Histol. Histopathol. 3:215-222.
40. Benowitz, N.L., and Jacob, P., III. 1984. Daily intake of nicotine during cigarette smoking. Clin. Pharmacol. Ther. 35:499-504.
41. Benowitz, N.L., Chan, K., Denaro, C.P., and Jacob, P. 1991. Stable isotope method for studying transdermal drug absorption: the nicotine patch. Clin. Pharmacol. Ther. 50:286-293.
42. Maritz, G.S., and Thomas, R.A. 1994. The influence of maternal nicotine exposure on the interalveolar septal status of neonatal rat lung. Cell Biol. Int. 18:747-757.
43. Orr-Urtreger, A., et al. 1997. Mice deficient in the alpha7 neuronal nicotinic acetylcholine receptor lack alpha-bungarotoxin binding sites and hippocampal fast nicotinic currents. J. Neurosci. 17:9165-9171.
44. Olale, F., Gerzanich, V., Kuryatov, A., Wang, F., and Lindstrom, J. 1997. Chronic nicotine exposure differentially affects the function of human α3, α4, and α7 neuronal nicotinic receptor subtypes. J. Pharmacol. Exp. Ther. 283:675-683.
45. Gray, R., Rajan, A.S., Radcliffe, K.A., Yakehiro, M. and Dani, J.A. 1996. Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature. 383:713-716.
46. McGehee, D.S., Heath, M.J., Gelber, S., Devay, P., and Role, L.W. 1995. Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science. 269:1692-1696.
47. Sekhon, H.S., Wright, J.L., and Churg, A. 1994. Cigarette smoke causes rapid cell proliferation in small airways and associated pulmonary arteries. Am. J. Physiol. 267:L557-L563.
48. Bearer, C., Emerson, R.K., O'Riordan, M.A., Roitman, E., and Shackleton, C. 1997. Maternal tobacco smoke exposure and persistent pulmonary hypertension of the newborn. Environ. Health Perspect. 105:202-206.
49. Conroy, W.G., and Berg, D.K. 1995. Neurons can maintain multiple classes of nicotinic acetylcholine receptors distinguished by different subunit compositions. J. Biol. Chem. 270:4424-4431.
50. Wang, F., et al. 1998. Chronic nicotine treatment upregulates human α3α2, but not α3α4 AChRs stably transfected in human embryonic kidney cells. J. Biol. Chem. 273:28721-28732.
51. Wuenschell, C.W., Zhao, J.S., Tefft, J.D., and Warburton, D. 1998. Nicotine stimulates branching and expression of SP-A and SP-C mRNAs in embryonic mouse lung culture. Am. J. Physiol. 274:L165-L170.
52. Lieberman, E., et al. 1992. Association of intrauterine cigarette smoke exposure with indices of fetal lung maturation. Obstet. Gynecol. 79:564-570.
53. Cutz, H., Perrin, D.G., Hackman, R., and Czegledy-Nagy, E.N. 1996. Maternal smoking and pulmonary neuroendocrine cells in sudden infant death syndrome. Pediatrics. 98:668-672.
54. Nylen, E.S., et al. 1993. Cholinergic-nicotinic control of growth and secretion of cultured pulmonary neuroendocrine cells. Anat. Rec. 236:129-135.
55. Khadempour, M.H., Ofulue, A.F., Sekhon, H.S., Cherukupalli, K.M., and Thurlbeck, W.M. 1992. Changes of growth hormone, somatomedin C, and bombesin following pneumonectomy. Exp. Lung Res. 18:421-432.