Prenatal cigarette smoke exposure effects on apoptotic and nicotinic acetylcholine receptor expression in the infant mouse brainstem

NeuroToxicology

Volumn 53, Issue , 2016, Pages 53-63

  Vivekanandarajah, Arunnjah ^a   Chan, Yik Lung ^c   Chen, Hui ^c   Machaalani, Rita ^a,b  

^a UNIVERSITY OF SYDNEY   (Australia)

^b SYDNEY CHILDREN'S HOSPITAL   (Australia)

^c UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

Author keywords

Caspase 3; Medulla; nAChR; Nicotine; Smoking chamber; Sudden infant death syndrome (SIDS); TUNEL

Indexed keywords

BUNGAROTOXIN RECEPTOR; CASPASE 3; CIGARETTE SMOKE; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR ALPHA2; NICOTINIC RECEPTOR ALPHA3; NICOTINIC RECEPTOR ALPHA4; NICOTINIC RECEPTOR ALPHA5; NICOTINIC RECEPTOR ALPHA9; NICOTINIC RECEPTOR BETA1; NICOTINIC RECEPTOR BETA2; UNCLASSIFIED DRUG; NICOTINE; PROTEIN SUBUNIT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CUNEATE NUCLEUS; ENZYME ACTIVATION; FACIAL NERVE NUCLEUS; FEMALE; GESTATIONAL AGE; HYPOGLOSSAL NUCLEUS; IMMUNOHISTOCHEMISTRY; INFANT; INFERIOR OLIVE; LACTATION; LATERAL RETICULAR NUCLEUS; MALE; MATING; MEDULLARY NUCLEUS; MOUSE; NONHUMAN; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMOKING; SOLITARY TRACT NUCLEUS; TRIGEMINAL NUCLEUS; TUNEL ASSAY; VAGUS NERVE DORSAL NUCLEUS; ADVERSE EFFECTS; ANALYSIS OF VARIANCE; ANIMAL; BRAIN STEM; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PATHOLOGY; PREGNANCY; PROTEIN SUBUNIT;

ANALYSIS OF VARIANCE; ANIMALS; APOPTOSIS; BRAIN STEM; CASPASE 3; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU NICK-END LABELING; MALE; MICE; NICOTINE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROTEIN SUBUNITS; RECEPTORS, NICOTINIC; SMOKING;

EID: 84952919559     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2015.12.017     Document Type: Article

References (107)

1. Abbott L.C., Winzer-Sehan U.H. Smoking during pregnancy: lessons learned from epidemiological studies and experimental studies using animal models. Crit. Rev. Toxicol. 2012, 42:279-303.
2. Albuquerque E., Pereira E.F.R., Alkondon M., Rogers S.W. Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol. Rev. 2009, 89:73-120.
3. Alm B., Lagercrantz H., Wennergren G. Stop SIDS-sleeping solitary supine, sucking soother, stopping smoking substitutes. Acta Paediatr. 2006, 95:260-262.
4. Alm B., Milerad J., Wennergren G., Skjærven R., Øyen N., Norvenius G., Daltveit A.K., Helweg-Larsen K., Markestad T., Irgens L.M. A case-control study of smoking and sudden infant death syndrome in the Scandinavian countries, 1992 to 1995. Arch. Dis. Child 1998, 78:329-334. on behalf of the Nordic Epidemiological SIDS Study.
5. Anderson H.R., Cook D.G. Passive smoking and sudden infant death syndrome: review of the epidemiological evidence. Thorax 1997, 52:1003-1009.
6. Bengtsson F., Hesslow G. Cerebellar control of the inferior olive. Cerebellum 2006, 5:7-14.
7. Benowitz N.L., Bernert J.T., Caraballo R.S., Holiday D.B., Wang J. Optimal serum cotinine levels for distinguishing cigarette smokers and nonsmokers within different racial/ethnic groups in the United States between 1999 and 2004. Am. J. Epidemiol. 2009, 169:236-248.
8. Berger F., Gage F.H., Vijayaraghavan S. Nicotinic receptor-induced apoptotic cell death of hippocampal progenitor cells. J. Neurosci. 1998, 18:6871-6881.
9. Bernstein I.M., Mongeon J.A., Badger G.J., Solomon L., Heil S.H., Higgins S.T. Maternal smoking and its association with birth weight. Obstet. Gynecol. 2005, 106:986-991.
10. Browne C.A., Colditz P.B., Dunster K.R. Infant autonomic function is altered by maternal smoking during pregnancy. Early Hum. Dev. 2000, 59:209-218.
11. Browne C.J., Sharma N., Water K.A., Machaalani R. The effects of nicotine on the alpha-7 and beta-2 nicotinic acetylcholine receptor subunits in the developing piglet brainstem. Int. J. Dev. Neurosci. 2010, 28:1-7.
12. Centeno M.L., Luo J., Lindstrom J.M., Caba M., Pau K.Y.F. Expression of α4 and α7 nicotinic receptors in the brainstem of female rabbits after coitus. Brain Res. 2004, 1012:1-12.
13. Cohen D.H., Schnall A.M. Medullary cells of origin of vagal cardioinhibitory fibers in the pigeon. II. Electrical stimulation of the dorsal motor nucleus. J. Comp. Neurol. 1970, 140:321-342.
14. Dampney R.A.L. Functional organization of central pathways regulating the cardiovascular system. Physiol. Rev. 1994, 74:323-364.
15. Di Angelantonio S., Matteoni C., Fabbretti E., Nistri A. Molecular biology and electrophysiology of neuronal nicotinic receptors of rat chromaffin cells. Eur. J. Neurosci. 2003, 17:2313-2322.
16. DiFranza J.R., Aligne C.A., Weitzman M. Prenatal and postnatal environmental tobacco smoke exposure and children's health. Pediatrics 2004, 113:1007-1015.
17. Duncan J.R., Garland M., Myers M.M., Fifer W.P., Yang M., Kinney H.C., Stark R.I. Prenatal nicotine-exposure alters fetal autonomic activity and medullary neurotransmitter receptors: implications for sudden infant death syndrome. J. Appl. Physiol. 2009, 107:1579-1590.
18. Dwyer J.B., McQuown S.C., Leslie F.M. The dynamic effects of nicotine on the developing brain. Pharmocol. Ther. 2009, 122:125-139.
19. Ellenberger H., Haselton J.R., Liskowsky D.R., Schneiderman N. The location of chronotropic cardioinhibitory vagal motoneurons in the medulla of the rabbit. J. Auton. Nerv. Syst. 1983, 9:513-529.
20. Falk L., Nordberg A., Seiger Å., Kjældgaard A., Hellström-Lindahl E. Smoking during early pregnancy affects the expression pattern of both nicotinic and muscarinic acetylcholine receptors in human first trimester brainstem and cerebellum. Neuroscience 2005, 132:389-397.
21. Falk L., Nordberg A., Seiger Å., Kjældgaard A., Hellström-Lindahl E. The α7 nicotinic receptor in human fetal brain and spinal cord. J. Neurochem. 2002, 80:457-465.
22. Fantuzzi G., Aggazzotti G., Righi E., Faccinetti F., Bertucci E., Kanitz S. Preterm delivery and exposure to active and passive smoking during pregnancy: a case-control study from Italy. Paediatr. Perinat. Epidemiol. 2007, 21:194-200.
23. Fregosi R.F., Fuller D.D. Respiratory-related control of extrinsic tongue muscle activity. Respir. Physiol. 1997, 110:295-306.
24. Gerzanich V., Anand R., Lindstrom J. Homopentamers of alpha 8 and alpha 7 subunits of nicotinic receptors exhibit similar channel but contrasting binding site properties. Mol. Pharmocol. 1994, 45:212-220.
25. Gilliland F.D., Li Y., Peters J.M. Effects of maternal smoking during pregnancy and environmental tobacco smoke on asthma and wheezing in children. Am. J. Respir. Crit. Care Med. 2001, 163:429-436.
26. Gotti C., Zoli M., Clementi F. Brain nicotinic acetylcholine receptors: native subtypes and their relevance. Trends Pharmocol. Sci. 2006, 27:482-491.
27. Gotti C., Clementi F. Neuronal nicotinic receptors: from structure to pathology. Prog. Neurobiol. 2004, 74:363-396.
28. Govind A.P., Walsh H., Green W.N. Nicotine-induced upregulation of native neuronal nicotinic receptors is caused by multiple mechanisms. J. Neurosci. 2012, 32:2227-2238.
29. Green C.R., Rodgman A. The Tobacco Chemists' Research Conference: a half century forum for advances in analytical methodology of tobaccos and its products. Rec. Adv. Tob. Sci. 1996, 22:131-304.
30. Hellstrom-Lindahl E., Gorbounova O., Seiger A., Mousavi M., Nordberg A. Regional distribution of nicotinic receptors during prenatal development of human brain and spinal cord. Brain Res. Dev. Brain Res. 1998, 108:147-160.
31. Hoffman H.J., Damus K., Hillman L., Krongrad E. Risk factors for SIDS. Results of the National Institute of Child Health and Human Development SIDS Cooperative Epidemiological Study. Ann. N. Y. Acad. Sci. 1988, 533:13-30.
32. Hofhuis W., Jongste J.C.De., Merkus P.J.F.M. Adverse health effects of prenatal and postnatal tobacco smoke exposure on children. Arch. Dis. Child 2003, 88:1086-1090.
33. Hogg R.C., Raggenbass M., Betrand D. Nicotinic acetylcholine receptors: from structure to brain function. Rev. Physiol. Biochem. Pharmacol. 2003, 147:1-46.
34. Hory-Lee F., Frank E. The nicotinic blocking agents d-tubocurare and alphabungarotoxin save motoneurons from naturally occurring death in the absence of neuromuscular blockade. J. Neurosci. 1995, 15:6453-6460.
35. Hu D., Cao K., Peterson-Wakeman R., Wang R. Altered profile of gene expression in rat hearts induced by chronic nicotine consumption. Biochem. Biophys. Res. Commun. 2002, 297:729-736.
36. Huang Z.G., Wang X., Dergacheva O., Mendelowitz D. Prenatal nicotine exposure recruits an excitatory pathway to brainstem parasympathetic cardioinhibitory neurons during hypoxia/hypercapnia in the rat: implications for sudden infant death syndrome. Pediatr. Res. 2005, 58:562-567.
37. Huang X.F., Tork I., Paxinos G. Dorsal motor nucleus of the vagus nerve: a cyto- and chemoarchitectonic study in the human. J. Comp. Neurol. 1993, 330:158-182.
38. Ilicali O.C., Keles N., Deier K., Saiun O.F., Guldiken Y. Evaluation of the effect of passive smoking on otitis media in children by and objective method: urinary cotinine analysis. Laryngoscope 2001, 111:163-167.
39. Jaiswal S.J., Pilarski J.Q., Harrison C.M., Fregosi R.F. Developmental nicotine exposure alters AMPA neurotransmission in the hypoglossal motor nucleus and pre-Botzinger complex of neonatal rats. J. Neurosci. 2013, 33:2616-2625.
40. Kabbani N., Levenson R. A proteomic approach to receptor signaling: molecular mechanisms and therapeutic implications derived from discovery of the dopamine D2 receptor signal plex. Eur. J. Pharmacol. 2007, 572:83-93.
41. Ke L., Eisenhour C.M., Bencherif M., Lukas R.J. Effects of chronic nicotine treatment on expression of diverse nicotinic acetylcholine receptor subtypes. I. Dose- and time-dependent effects of nicotine treatment. J. Pharmacol. Exp. Ther. 1998, 286:825-840.
42. Kurzen H., Berger H., Jager C., Hartschuh W., Naher H., Gratchev A., Goerdt S., Deichmann M. Phenotypical and molecular profiling of the extraneuronal cholinergic system of the skin. J. Invest. Dermatol. 2004, 123:937-949.
43. Labarca C., Schwarz J., Deshpande P., Schwarz S., Nowak M.W., Fonck C., Nashmi R., Kofuji P., Dang H., Shi W., Fidan M., Khakh B.S., Chen Z., Bowers B.J., Boulter J., Wehner J.M., Lester H.A. Point mutant mice with hypersensitive alpha 4 nicotinic receptors show dopaminergic deficits and increased anxiety. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:2786-2791.
44. Lambers D.S., Clark K.E. The maternal and fetal physiologic effects of nicotine. Semin. Perinatol. 1996, 20:115-126.
45. Lang P.M., Burgstahler R., Sippel W., Irnich D., Schlotter-Weigel B., Grafe P. Characterization of neuronal nicotinic acetylcholine receptors in the membrane of unmyelinated human C-fiber axons by in vitro studies. J. Neurophysiol. 2003, 90:3295-3303.
46. Larsson M., Montgomery S.M. Maternal smoking during pregnancy and physical control and coordination among offspring. J. Epidemiol. Community Health 2011, 65:1151-1158.
47. Lei F., Yan X., Zhao F., Zhang S., Zhang Q., Zhou H. Impairment of central chemoreception in neonatal rats induced by maternal cigarette smoke exposure during pregnancy. PLoS One 2015, 10(9):e0137362. 10.1371/journal.pone.0137362.
48. Liu J., Sakurai R., O'Roark E.M., Kenyon N.J., Torday J.S., Rehan V.K. PPARγ agonist rosiglitazone prevents perinatal nicotine exposure-induced asthma in rat offspring. Am. J. Physiol. Lung Cell. Mol. Physiol. 2011, 300:710-717.
49. Llinas R., Walton K., Hillman D.E., Sotelo C. Inferior olive: its role in motor learning. Science 1975, 190:1230-1231.
50. Luck W., Nau H. Nicotine and cotinine concentrations in serum and urine of infants exposed via passive smoking or milk from smoking mothers. J. Pediatr. 1985, 107:816-820.
51. Lv J., Mao C., Zhu L., Zhang H., Pengpeng H., Xu F., Liu Y., Zhang L., Xu Z. The effect of prenatal nicotine on expression of nicotine receptor subunits in the fetal brain. Neurotoxicology 2008, 29:722-726.
52. Machaalani R., Ghazavi E., Hinton T., Waters K.A., Hennessy A. Cigarette smoking during pregnancy regulates the expression of specific nicotinic acetylcholine receptor (nAChR) subunits in the human placenta. Toxicol. Appl. Pharm. 2014, 276:204-212.
53. Machaalani R., Say M., Waters K.A. Effects of cigarette smoke exposure on nicotinic acetylcholine receptor subunits α7 and β2 in the sudden infant death syndrome (SIDS) brainstem. Toxicol. Appl. Pharm. 2011, 257:369-404.
54. Machaalani R., Kashi P.K., Waters K.A. Distribution of nicotinic acetylcholine receptor subunits α7 and β2 in the human brainstem and hippocampal formation. J. Chem. Neuroanat. 2010, 40:223-231.
55. Machaalani R., Waters K.A. Neuronal cell death in the Sudden Infant Death Syndrome brainstem and associations with risk factors. Brain 2008, 131:218-228.
56. Machaalani R., Rodriguez M., Waters K.A. Active caspase-3 in the sudden infant death syndrome (SIDS) brainstem. Acta Neuropathol. 2007, 113:577-584.
57. Machaalani R., Waters K.A., Tinworth K.D. Effects of postnatal nicotine exposure on apoptotic markers in the developing piglet brain. Neuroscience 2005, 132:325-333.
58. Marks M.J., Pauly J.F.L., Gross S.D., Deneris E.S., Hermans-Borgmeyer I., Heinemann S.F., Collins A.C. Nicotine binding and nicotinic receptor subunit RNA after chronic nicotine treatment. J. Neurosci. 1992, 12:2765-2784.
59. McIntosh J.M., Absalom N., Chebib M., Elgoyhen A.B., Vincler M. Alpha 9 nicotinic acetylcholine receptors and the treatment of pain. Biochem. Pharmacol. 2009, 78:693-702.
60. Mielke J.G., Mealing G.A. Cellular distribution of the nicotinic acetylcholine receptor alpha7 subunit in rat hippocampus. Neurosci. Res. 2009, 65:296-306.
61. Mitchell E.A., Taylor B.J., Ford R.P., Stewart A.W., Becroft D.M., Thompson J.M., Scragg R., Hassall I.B., Barry D.M., Allen E.M. Dummies and the sudden infant death syndrome. Arch. Dis. Child 1993, 68:501-504.
62. Naeff B., Schlumpf M., Lichtensteiger W. Prenatal and post- natal development of high-affinity H3 nicotine binding sites in rat brain regions: an autoradiographic study. Dev. Brain Res. 1992, 68:163-174.
63. Neff R.A., Simmens S.J., Evans C., Mendelowitz D. Prenatal nicotine exposure alters central cardiorespiratory responses to hypoxia in rats: implications for sudden infant death syndrome. J. Neurosci. 2004, 24:9261-9268.
64. Nikolaev A.1, McLaughlin T., O'Leary D.D., Tessier-Lavigne M. APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature 2009, 457(7232):981-989.
65. Onal A., Uysal A., Ulker S., Delen Y., Yurtseven M.E., Evinc A. Alterations of brain tissue in fetal rats exposed to nicotine in utero: possible involvement of nitric oxide and catecholamines. Neurotoxicol. Teratol. 2004, 26:103-112.
66. Orr-Urtreger A., Broide R.S., Kasten M.R., Dang H., Dani J.A., Beaudet A.L., Patrick J.W. Mice homozygous for the L250T mutation in the alpha 7 nicotinic acetylcholine receptor show increased neuronal apoptosis and die within 1day of birth. J. Neurochem. 2000, 74:2154-2166.
67. Oshikawa J., Toya Y., Fujita T., Egawa M., Kawabe J., Umemura S., Ishikawa Y. Nicotinic acetylcholine receptor α7 regulates cAMP signal within lipid rafts. Am. J. Physiol. Cell Physiol. 2003, 285:567-574.
68. Paulo J., Brucker W., Hawrot E. Proteomic analysis of an alpha7 nicotinic acetylcholine receptor interactome. J. Proteome Res. 2009, 8:1849-1858.
69. Paxinos G., Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates 2004, Compact ed Academic, London. 2nd ed.
70. Perry D.C., Xiao Y., Nguyen H.N., Musachio J.L., Davila-Garcia M.I., Kellar K.J. Measuring nicotinic receptors with characteristics of α4β2, α3β2 and α3β4 subtypes in rat tissues by autoradiography. J. Neurochem. 2002, 82:468-481.
71. Pilarski J.Q., Wakefield H.E., Fuglevand A.J., Levine R.B., Fregosi R.F. Developmental nicotine exposure alters neurotransmission and excitability in hypoglossal motoneurons. J. Neurophysiol. 2011, 105:423-433.
72. Pollock V.V., Pastoor T.E., Wecker L. Cyclic AMP-dependent protein kinase (PKA) phosphorylates Ser362 and 467 and protein kinase C phosphorylates Ser550 within the M3/M4 cytoplasmic domain of human nicotinic receptor alpha4 subunits. J. Neurochem. 2007, 103:456-466.
73. Powell G.L., Levine R.B., Frazier A.M., Fregosi R.F. Influence of developmental nicotine exposure on spike-timing precision and reliability in hypoglossal motoneurons. J. Neurophysiol. 2015, 113:1862-1872.
74. Quitadamo C., Fabbretti E., Lamanauskas N., Nistri A. Activation and desensitization of neuronal nicotinic receptors modulate glutamatergic transmission on neonatal rat hypoglossal motoneurons. Eur. J. Neurosci. 2005, 22:2723-2734.
75. Remmers J.E., DeGroot W.J., Sauerland E.K., Anch A.M. Pathogenesis of upper airway occlusion during sleep. J. Appl. Physiol. 1978, 44:931-938.
76. Renshaw G., Rigby P., Self G., Lamb A., Goldie R. Exogenously administered alpha-bungarotoxin binds to embryonic chick spinal cord: implications for the toxin-induced arrest of naturally occurring motoneuron death. Neuroscience 1993, 53:1163-1172.
77. Rondi-Reig L., Delhaye-Bouchaud N., Mariani J., Caston J. Role of the inferior olivary complex in motor skills and motor learning in the adult rat. Neuroscience 1997, 77:955-963.
78. Roy T.S., Andrews J.E., Seidler F.J., Slotkin T.A. Nicotine evokes cell death in embryonic rat brain during neurulation. J. Pharmocol. Exp. Ther. 1998, 287:1136-1144.
79. Rudell J.C., Borges L.S., Rudell J.B., Beck K.A., Ferns M.J. Determinants in the β and δ subunit cytoplasmic loop regulate Golgi trafficking and surface expression of the muscle acetylcholine receptor. J. Biol. Chem. 2014, 289:203-214.
80. Scheffer D., Sage C., Plazas P.V., Huang M., Wedemeyer C., Zhang D.S., Chen Z.Y., Elgoyhen A.B., Corey D.P., Pingault V. The α1 subunit of nicotinic acetylcholine receptors in the inner ear: transcriptional regulation by ATOH1 and co-expression with the ã subunit in hair cells. J. Neurochem. 2007, 103(6):2651-2664.
81. Simakajornboon N., Kuptanon T., Jirapongsuwan P. The effect of prenatal nicotine exposure on PDGFR-mediated anti-apoptotic mechanism in the caudal brainstem of developing rat. Neurosci. Lett. 2010, 478:46-50.
82. Slotkin T.A., Skavicus S., Card J., Stadler A., Levin E.D., Seidler F.J. Developmental neurotoxicity of tobacco smoke directed toward cholinergic and serotonergic systems: more than just nicotine. Toxicol. Sci. 2015, 147:178-189.
83. Slotkin T.A., Seidler F.J., Qiao D., Aldridge J.E., Tate C.A., Cousins M.M., Proskocil B.J., Sekhon H.S., Clark J.A., Lupo S.L., Spindel E.R. Effects of prenatal nicotine exposure on primate brain development and attempted amelioration with supplemental choline or vitamin C: neurotransmitter receptors, cell signaling and cell development biomarkers in fetal brain regions of rhesus monkeys. Neuropsychopharmacology 2005, 30:129-144.
84. Slotkin T.A., Pinkerton K.E., Auman J.T., Qiao D., Seidler F.J. Perinatal exposure to environmental tobacco smoke up regulates nicotinic cholinergic receptors in monkey brain. Dev. Brain Res. 2002, 133:175-179.
85. Slotkin T.A. Developmental cholinotoxicants: nicotine and chlorpyrifos. Environ. Health Perspect. 1999, 107:71-80.
86. Slotkin T.A. Fetal nicotine or cocaine exposure: which one is worse?. J. Pharmacol. Exp. Ther. 1998, 285:931-945.
87. Slotkin T.A., Saleh J.L., McCook E.C., Seidler F.J. Impaired cardiac function during postnatal hypoxia in rats exposed to nicotine prenatally: implications for perinatal morbidity and mortality, and for sudden infant death syndrome. Teratology 1997, 55:177-184.
88. Slotkin T.A., McCook E.C., Seidler F.J. Cryptic brain cell injury caused by fetal nicotine exposure is associated with persistent elevations of c-fos protooncogene expression. Brain Res. 1997, 750:180-188.
89. Slotkin T.A., Lappi S.E., Seidler F.J. Impact of fetal nicotine exposure on development of rat brain regions: critical sensitive periods or effects of withdrawal?. Brain Res. Bull. 1993, 31:319-328.
90. Slotkin T.A., Orband-Miller L., Queen K.L., Whitmore W.L., Seidler F.J. Effects of prenatal nicotine exposure on biochemical development of rat brain regions: maternal drug infusions via osmotic minipumps. J. Pharmocol. Exp. Ther. 1987, 240:602-611.
91. Sovik S., Lossius K., Walloe L. Heart rate response to transient chemoreceptor stimulation in term infants is modified by exposure to maternal smoking. Pediatr. Res. 2001, 49:558-565.
92. Stecco C., Porzionato A., Macchi V., Sarasin G., Calcagno A., Parenti A. Detection of apoptosis in human brainstem by TUNEL assay. Ital. J. Anat. Embryol. 2005, 110:255-260.
93. Su A.I., Cooke M.P., Ching K.A., Hakak Y., Walker J.R., Wiltshire T., Orth A.P., Vega R.G., Sapinoso L.M., Moqrich A., Patapoutian A., Hampton G.M., Schultz P.G., Hogenesch J.B. Large- scale analysis of the human and mouse transcriptomes. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:4465-4470.
94. Thiriez G., Bouhaddi M., Mourot L., Nobili F., Fortrat J.O., Menget A., Franco P., Regnard J. Heart rate variability in preterm infants and maternal smoking during pregnancy. Clin. Auton. Res. 2009, 19:149-156.
95. Tolson C.M., Seidler F.J., Mccook E.C., Slotkin T.A. Does concurrent or prior nicotine exposure interact with neonatal hypoxia to produce cardiac cell damage?. Teratology 1995, 52:298-305.
96. Tournier J.M., Maouche K., Coraux C., Zahm J.M., Cloez-Tayarani I., Nawrocki-Raby B., Bonnomet A., Burlet H., Lebargy F., Polette M., Birembaut P. alpha3alpha5beta2-Nicotinic acetylcholine receptor contributes to the wound repair of the respiratory epithelium by modulating intracellular calcium in migrating cells. Am. J. Pathol. 2006, 168:55-68.
97. Trasti N., Vik T., Jacobsen G., Bakketeig L.S. Smoking in pregnancy and children's mental and motor development at age 1 and 5 years. Early Hum. Dev. 1999, 55:137-147.
98. Tribollet E., Bertrand D., Marguerat A., Raggenbass M. Comparative distribution of nicotinic receptor subtypes during development, adulthood and aging: an autoradiographic study in the rat brain. Neuroscience 2004, 124:405-420.
99. Ueda Y., Stick S.M., Hall G., Sly P. Control of breathing in infants born to smoking mothers. J. Pediatr. 1999, 135:226-232.
100. Vivekanandarajah A., Waters K.A., Machaalani R. Postnatal nicotine effects on the expression of nicotinic acetylcholine receptors in the developing piglet hippocampus and brainstem. Int. J. Dev. Neurosci. 2015, 9:183-191.
101. West K.A., Brognard J., Clark A.S., Linnoila I.R., Yang X., Swain S.M., Harris C., Belinsky S., Dennis P.A. Rapid Akt activation by nicotine and a tobacco carcinogen modulates the phenotype of normal human airway epithelial cells. J. Clin. Inevst. 2003, 111:81-90.
102. Whiteaker P., Cooper J.F., Salminen O., Marks M.J., McClure-Begley T.D., Brown R.W., Collins A.C., Lindstrom J.M. Immunolabeling demonstrates the interdependence of mouse brain alpha4 and beta2 nicotinic acetylcholine receptor subunit expression. J. Comp. Neurol. 2006, 499:1016-1038.
103. Wisborg K., Kesmodel U., Henriksen T.B., Olsen S.F., Secher N.J. Exposure to tobacco smoke in utero and the risk of stillbirth and death in the first year of life. Am. J. Epidemiol. 2001, 154:322-327.
104. Woolf C.J. The pathophysiology of peripheral neuropathic pain-abnormal peripheral input and abnormal central processing. Acta Neurochir. Suppl. (Wien) 1993, 58:125-130.
105. Xu W., Gelber S., Orr-Urtreger A., Armstrong D., Lewis R.A., Ou C.N., Patrick J., Role L., DeBiasia M., Beaudet A.L. Megacystis, mydriasis, and ion channel defect in mice lacking the alpha3 neuronal nicotinic acetylcholine receptor. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:5746-5751.
106. Yu W.F., Guan Z.Z., Nordberg A. Postnatal upregulation of α4 and α3 nicotinic receptor subunits in the brain of α7 nicotinic receptor-deficient mice. Neuroscience 2007, 146:1618-1628.
107. Zeidler R., Albermann K., Lang S. Nicotine and apoptosis. Apoptosis 2007, 12:1927-1943.