Postnatal nicotine effects on the expression of nicotinic acetylcholine receptors in the developing piglet hippocampus and brainstem

International Journal of Developmental Neuroscience

Volumn 47, Issue , 2015, Pages 183-191

  Vivekanandarajah, Arunnjah ^a,b   Waters, Karen A ^a,b,c   Machaalani, Rita ^a,b,c  

^a Bosch Institute   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c SYDNEY CHILDREN'S HOSPITAL   (Australia)

Author keywords

Brain; Cigarette; Immunohistochemistry; Protein; Sudden Infant Death Syndrome

Indexed keywords

BUNGAROTOXIN RECEPTOR; NICOTINE; 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; NICOTINIC AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN FUNCTION; BRAIN STEM; CARDIORESPIRATORY CONTROL; COGNITION; CONTROLLED STUDY; DEVELOPMENTAL TOXICITY; FEMALE; HEART FUNCTION; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA2 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; HYPOGLOSSAL NUCLEUS; IMMUNOHISTOCHEMISTRY; MALE; MEDULLA OBLONGATA; NEUROANATOMY; NEUROTOXICITY; NONHUMAN; PERINATAL DRUG EXPOSURE; PIGLET; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RESPIRATION CONTROL; SPINAL TRIGEMINAL TRACT NUCLEUS; VAGUS NERVE DORSAL NUCLEUS; VESTIBULAR NUCLEUS; AGE; ANIMAL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MINIPIG; NEWBORN; PIG;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BRAIN STEM; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIPPOCAMPUS; MALE; NICOTINE; NICOTINIC AGONISTS; RECEPTORS, NICOTINIC; SWINE; SWINE, MINIATURE;

EID: 84945271326     PISSN: 07365748     EISSN: 1873474X     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2015.09.007     Document Type: Article

References (91)

1. 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.
2. Andresen M.C., Kunze D.L. Nucleus tractus solitarius-gateway to neural circulatory control. Annu. Rev. Physiol. 1994, 56:93-116.
3. Bauman K.E., Flewelling R.L., LaPrelle J. Parental cigarette smoking and cognitive performance of children. Health Psychol. 1991, 10:282-288.
4. Bejjani C., Machaalani R., Waters K.A. The dorsal motor nucleus of the vagus in the Sudden Infant Death Syndrome. Respir. Physiol. Neurobiol. 2013, 185:203-210.
5. Biallas S., Wilker S., Lips K.S., Kummer W., Grando S.A., Padberg W., Grau V. Immunohistochemical detection of nicotinic acetylcholine receptor subunits α9 and α10 in rat lung isografts and allografts. Life Sci. 2007, 80:2286-2289.
6. 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.
7. Chen R., Clifford A., Lang L., Anstey K.J. Is exposure to secondhand smoke associated with cognitive parameters of children and adolescents? A systematic literature review. Ann. Epidemiol. 2013, 23:652-661.
8. Cho S.C., Kim B.N., Hong Y.C., Shin M.S., Yoo H.J., Kim J.W. Effect of environmental exposure to lead and tobacco smoke on inattentive and hyperactive symptoms and neurocognitive performance in children. J. Child Psychol. Psychiatry 2010, 51:1050-1057.
9. Colomer C., Olivos-Ore L.A., Vincent A., McIntosh J.M., Artalejo A.R., Guerineau N.C. Functional characterization of alpha9-containing cholinergic nicotinic receptors in the rat adrenal medulla: implication in stress-induced functional plasticity. J. Neurosci. 2010, 30:6732-6742.
10. Committee on Environmental Health Environmental tobacco smoke: a hazard to children. Pediatrics 1997, 99:639-642.
11. Constantin E., Waters K.A., Morielli A., Brouillette R.T. Head turning and face-down positioning in prone-sleeping premature infants. J. Pediatr. 1999, 134:558-562.
12. Cook D., Strachan D. Health effects of passive smoking 3: parental smoking and prevalence of respiratory symptoms and asthma in school age children. Thorax 1997, 52:1081-1094.
13. Dampney R.A.L. Functional organization of central pathways regulating the cardiovascular system. Physiol. Rev. 1994, 74:323-364.
14. Del Mar Arroyo-Jiménez M., Bourgeois J.-P., Marubio L.M., Le Sourd A.-M., Ottersen O.P., Rinvik E., Fairén A., Changeux J.P. Ultrastructural localization of the α4 subunit of the neuronal acetylcholine nicotinic receptor in the rat substantia nigra. J. Neurosci. 1999, 19:6475-6487.
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. DiFranza J.R., Lew R.A. Morbidity and mortality in children associated with the use of tobacco products by other people. Pediatrics 1996, 97:560-568.
18. Dobbing J., Sands J. Comparative aspects of brain growth spurts. Early Hum. Dev. 1979, 311:79-83.
19. Dominguez del Toro E., Juiz J.M., Peng X., Lindstrom J., Criado M. Immunocytochemical localization of the alpha 7 subunit of the nicotinic acetylcholine receptor in the rat central nervous system. J. Comp. Neurol. 1994, 349:325-342.
20. Duncan J.R., Randall L.L., Belliveau R.A., Trachtenberg F.L., Randall B., Habbe D., Mandell F., Welty T.K., Iyasu S., Kinney H.C. The effect of maternal smoking and drinking during pregnancy upon (3)H-nicotine receptor brainstem binding in infants dying of the sudden infant death syndrome: initial observations in a high risk population. Brain Pathol. 2008, 18:21-31.
21. Dwyer J.B., McQuown S.C., Leslie F.M. The dynamic effects of nicotine on the developing brain. Pharmocol. Ther. 2009, 122:125-139.
22. Eriksson P., Ankarberg E., Fredriksson A. Exposure to nicotine during a defined period in neonatal life induces permanent changes in brain nicotinic receptors and in behaviour of adult mice. Brain Res. 2000, 853:41-48.
23. Ey J.L., Holberg C.J., Aldous M.B., Wright A.L., Martinez F.D., Taussig L.M. Passive smoke exposure and otitis media in the first year of life. Pediatrics 1995, 95:670-677.
24. Felix B., Leger M.E., Albe-Fessard D., Marcilloux J.C., Rampin O., Laplace J.P. Stereotaxic atlas of the pig brain. Brain Res. Bull. 1999, 49:1-137.
25. Gerzanich V., Anand R., Lindstrom J. Homomers of alpha 8 and alpha 7 subunits of nicotinic receptors exhibit similar channel but contrasting binding site properties. Mol. Pharmacol. 1994, 45:212-220.
26. Getz R., Sirnes T. The localization within the dorsal motor vagal nucleus. An experimental investigation. J. Comp. Neurol. 1949, 90:95-110.
27. Gotti C., Clementi F. Neuronal nicotinic receptors: from structure to pathology. Prog. Neurobiol. 2004, 74:363-396.
28. Gotti C., Zoli M., Clementi F. Brain nicotinic acetylcholine receptors: native subtypes and their relevance. Trends Pharmocol. Sci. 2006, 27:482-491.
29. 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.
30. Gray R., Rajan A.S., Radcliffe K.A., Yakehiro M., Dani J.A. Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 1996, 383:713-716.
31. 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.
32. Haberg S.E., Stigum H., Nystad W., Nafstad P. Effects of pre- and postnatal exposure to parental smoking on early childhood respiratory health. Am. J. Epidemiol. 2007, 166:679-686.
33. Hall S.M., Haworth S.G. Normal adaptation of pulmonary arterial intima to extrauterine life in the pig: ultrastructural studies. J. Pathol. 1986, 149:55-66.
34. Han Z.Y., Le Novère N., Zoli M., Hill J.A., Champtaux N., Changeux J.P. Localisation of nAChR subunit mRNAs in the brain of Macaca mulatta. Eur. J. Neurosci. 2000, 12:3664-3674.
35. Huang L.Z., Winzer-Sehan U.H. Chronic neonatal nicotine upregulates heteromeric nicotinic acetylcholine receptor binding without change in subunit mRNA expression. Brain Res. 2006, 1113:94-109.
36. Huang L.Z., Abbott C., Winzer-Sehan U.H. Effects of chronic nicotine exposure on nicotinic acetylcholine receptor binding, cell death and morphology in hippocampus and cerebellum. Neuroscience 2007, 146:1854-1868.
37. Hunt C.E. Sudden infant death syndrome. Respiratory Control Disorders in Infants and Children 1992, 190-211. Williams and Wilkins, Sydney. R.C. Beckerman, R.T. Brouillette, C.E. Hunt (Eds.).
38. Hunter B.E., de Fiebre C.M., Papke R.L., Kem W.R., Meyer E.M. A novel nicotinic agonist facilitates induction of long-term potentiation in the rat hippocampus. Neurosci. Lett. 1994, 168:130-134.
39. Jones S., Sudweeks S., Yakel J.L. Nicotinic receptors in the brain: correlating physiology with function. Trends Neurosci. 1999, 22:555-561.
40. Kabbani N., Levenson R. A proteomic approach to receptor signaling: molecular mechanisms and therapeutic implications derived from discovery of the dopamine [2D] receptor signalplex. Eur. J. Pharmacol. 2007, 572:83-93.
41. Katz D.M., Karten H.J. Topographic representation of visceral target organs within the dorsal motor nucleus of the vagus nerve of the pigeon, columba livia. J. Comp. Neurol. 1985, 242:397-414.
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. 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.
44. Levin E.D. Nicotinic systems and cognitive function. Psychopharmacology 1992, 108:417-431.
45. Liebrechts-Akkerman G., Lao O., Liu F., van Sleuwen B.E., Engelberts A.C., L'Hoir M.P., Tiemeier H.W., Kayser M. Postnatal parental smoking: an important risk factor for SIDS. Eur. J. Pediatr. 2011, 170:1281-1291.
46. Lips K.S., Bruggmann D., Pfeil U., Vollerthun R., Grando S.A., Kummer W. Nicotinic acetylcholine receptors in rat and human placenta. Placenta 2005, 26:735-746.
47. 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.
48. 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.
49. Martin-Ruiz C.M., Piggott M., Gotti C., Lindstrom J., Mendelow A.D., Siddique M.S., Perry R.H., Perry E.K., Court J.A. Alpha and Beta nicotinic acetylcholine receptor subunits and synaptophysin in putamen from Parkinson's disease. Neuropharmacology 2000, 39:2830-2839.
50. 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.
51. 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.
52. 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.
53. Machaalani R., Waters K.A., Tinworth K.D. Effects of postnatal nicotine exposure on apoptotic markers in the developing piglet brain. J. Neurosci. 2005, 132:325-333.
54. Machaalani R., Waters K.A. NMDA receptor 1 expression in the brainstem of human infants and its relevance to the sudden infant death syndrome (SIDS). J. Neuropathol. Exp. Neurol. 2003, 62:1076-1085.
55. Maison S.F., Luebke A.E., Liberman M.C., Zuo J. Efferent protection from acoustic injury is mediated via α9 nicotinic acetylcholine receptors on outer hair cells. J. Neurosci. 2002, 22:10838-10846.
56. 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.
57. Matsuoka I., Domino E.F. Cholinergic mechanisms in the cat vestibular system. Neuropharmacology 1975, 14:201-210.
58. McCrea R., Gdowski G., Luan H. Current concepts of vestibular nucleus function. Ann. N. Y. Acad. Sci. 2001, 942:328-344.
59. McCrea R.A. Neuroanatomy of the oculomotor system. The nucleus prepositus. Rev. Oculomotor Res. 1988, 2:203-223.
60. McGehee D.S., Role L.W. Memories of nicotine. Nature 1996, 383:670-671.
61. Miao H., Liu C., Bishop K., Gong Z.H., Nordberg A., Zhang X. Nicotine exposure during a critical period of development leads to persistent changes in nicotinic acetylcholine receptors of adult rat brain. J. Neurochem. 1998, 70:752-762.
62. Mielke J.G., Mealing G.A. Cellular distribution of the nicotinic acetylcholine receptor alpha7 subunit in rat hippocampus. Neurosci. Res. 2009, 65:296-306.
63. Nachmanoff D.B., Panigrahy A., Filiano J.J., Mandell F., Sleeper L.A., Valdes-Dapena M., Krous H.F., White W.F., Kinney H.C. Brainstem 3H-nicotine receptor binding in the sudden infant death syndrome. J. Neuropathol. Exp. Neurol. 1998, 57:1018-1025.
64. Nara T., Goto N., Hamano S. Development of the human dorsal nucleus of vagus nerve: a morphometric study. J. Auton. Nerv. Syst. 1991, 33:267-275.
65. Nordberg A., Zhang X., Fredriksson A., Eriksson P. Neonatal nicotine exposure induces permanent changes in brain nicotinic receptors and behaviour in adult mice. Dev. Brain Res. 1991, 63:201-207.
66. Nolte J., Angevine J.B. The Human Brain in Photographs and Diagrams 1995, Mosby, St. Louis.
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. Owen M.J., Baldwin C.D., Swank P.R., Pannu A.K., Johnson D.L., Howie V.M. Relation of infant feeding practices, cigarette smoke exposure, and group child care to the onset and duration of otitis media with effusion in the first two years of life. J. Pediatr. 1993, 123:702-711.
69. Paulo J., Brucker W., Hawrot E. Proteomic analysis of an alpha7 nicotinic acetylcholine receptor interactome. J. Proteome Res. 2009, 8:1849-1858.
70. Paxinos G., Huang X. Atlas of the Human Brainstem 1995, Academic Press, California.
71. Poirier M.F., Canceil O., Baylé F., Millet B., Bourdel M.C., Moatti C., Olié J.P., Attar-Lévy D. Prevalence of smoking in psychiatric patients. Prog. Neuropsychopharmacol. Biol. Psychiatry 2002, 26:529-537.
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. Quik M., Polonskaya Y., Gillespie A., Jakowec M., Lloyd G.K., Langston J.W. Localization of nicotinic receptor subunit mRNAs in monkey brain by in situ hybridization. J. Comp. Neurol. 2000, 425:58-69.
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. Rothlin C.V., Lioudyno M.I., Silbering A.F., Plazas P.V., Casati M.E., Katz E., Guth P.S., Elgoyhen A.B. Direct interaction of serotonin type 3 receptor ligands with recombinant and native alpha 9 alpha 10-containing nicotinic cholinergic receptors. Mol. Pharmacol. 2003, 63:1067-1074.
76. Romijn H.J., Hofman M.A., Gramsbergen A. At what age is the developing cerebral cortex of the rat comparable to that of the full-term newborn human baby?. Early Hum. Dev. 1991, 26:61-67.
77. Sawada S., Yamamoto C., Ohno-Shosaku T. Long-term potentiation and depression in the dentate gyrus, and effects of nicotine. Neurosci. Res. 1994, 20:323-329.
78. 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 subunit in hair cells. J. Neurochem. 2007, 103:2651-2664.
79. Schneider J., Mitchell I., Singhal N., Kirk V., Hasan S.U. Prenatal cigarette smoke exposure attenuates recovery from hypoxemic challenge in preterm infants. Am. J. Respir. Crit. Care Med. 2008, 178:520-526.
80. Scott S.C., Inman J.D., Moss I.R. Ontogeny of sleep/wake and cardiorespiratory behavior in unanesthetized piglets. Respir. Physiol. 1990, 80:83-101.
81. Slotkin T.A. Fetal nicotine or cocaine exposure: which one is worse. J. Pharmacol. Exp. Ther. 1998, 285:931-945.
82. Spyer K.M. Central nervous mechanisms contributing to cardiovascular control. J. Physiol. 1994, 474:1-19.
83. Strachan D.P., Cook D.G. Parental smoking, middle ear disease and adenotonsillectomy in children. Thorax 1998, 53:50-56.
84. Teaktong T., Graham A., Court J., Perry R., Jaros E., Johnson M., Hall R., Perry E. Alzheime's disease is associated with a selective increase in α7 nicotinic acetylcholine receptor immunoreactivity in astrocytes. Glia 2003, 41:207-211.
85. 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.
86. Verbitsky M., Rothlin C.V., Katz E., Elgoyhen A.B. Mixed nicotinic-muscarinic properties of the alpha9 nicotinic cholinergic receptor. Neuropharmacology 2000, 39:2515-2524.
87. Vetter D.E., Liberman M.C., Mann J., Barhanin J., Boulter J., Brown M.C., Saffiote-Kolman J., Heinemann S.F., Elgoyhen A.B. Role of α9 nicotinic ach receptor subunits in the development and function of cochlear efferent innervation. Neuron 1999, 23:93-103.
88. 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.
89. Winzer-Serhan U., Leslie F.M. Expression of α5 nicotinic acetylcholine receptor subunit mRNA during hippocampal and cortical development. J. Comp. Neurol. 2005, 481:19-30.
90. 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.
91. Zaninetti M., Tribollet E., Bertrand D., Raggenbass M. Presence of functional neuronal nicotinic acetylcholine receptors in brainstem motorneurons of the rat. Eur. J. Neurosci. 1999, 11:2737-2748.