Increased nicotinic receptor desensitization in hypoglossal motor neurons following chronic developmental nicotine exposure

Journal of Neurophysiology

Volumn 107, Issue 1, 2012, Pages 257-264

  Pilarski, Jason Q ^a   Wakefield, Hilary E ^a   Fuglevand, Andrew J ^a   Levine, Richard B ^a   Fregosi, Ralph F ^a  

^a UNIVERSITY OF ARIZONA   (United States)

Author keywords

Obstructive sleep apnea; Tongue

Indexed keywords

NICOTINE; NICOTINIC RECEPTOR; RIVANICLINE;

ARTICLE; CONTROLLED STUDY; DESENSITIZATION; DEVELOPMENTAL NICOTINE EXPOSURE; EXPOSURE; HYPOGLOSSAL NERVE; MOTONEURON; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NEUROMODULATION; NEWBORN; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RAT;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; FEMALE; HYPOGLOSSAL NERVE; MALE; MEDULLA OBLONGATA; MOTOR NEURONS; NICOTINE; NICOTINIC ANTAGONISTS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RECEPTORS, NICOTINIC;

EID: 84255182566     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00623.2011     Document Type: Article

References (83)

1. Bamford OS, Carroll JL. Dynamic ventilatory responses in rats: normal development and effects of prenatal nicotine exposure. Respir Physiol 117: 29-40, 1999.
2. Bamford OS, Schuen JN, Carroll JL. Effect of nicotine exposure on postnatal ventilatory responses to hypoxia and hypercapnia. Respir Physiol 106: 1-11, 1996.
3. Barik J, Wonnacott S. Molecular and cellular mechanisms of action of nicotine in the CNS. Hand Exp Pharmacol 192: 173-207, 2009.
4. Bencherif M, Lovette ME, Fowler KW, Arrington S, Reeves L, Caldwell WS, Lippiello PM. RJR-2403: a nicotinic agonist with CNS selectivity I. In vitro characterization. J Pharmacol Exp Ther 279: 1413-1421, 1996.
5. Boudinot E, Yamada M, Wess J, Champagnat J, Foutz AS. Ventilatory pattern and chemosensitivity in M1 and M3 muscarinic receptor knockout mice. Respir Physiol Neurobiol 139: 237-245, 2004.
6. Buisson B, Bertrand D. Chronic exposure to nicotine upregulates the human (alpha)4(beta)2 nicotinic acetylcholine receptor function. J Neurosci 21: 1819-1829, 2001.
7. Buisson B, Vallejo YF, Green WN, Bertrand D. The unusual nature of epibatidine responses at the alpha4beta2 nicotinic acetylcholine receptor. Neuropharmacology 39: 2561-2569, 2000.
8. Calabresi P, Lacey MG, North RA. Nicotinic excitation of rat ventral tegmental neurones in vitro studied by intracellular recording. Br J Pharmacol 98: 135-140, 1989.
9. Chamberlin NL, Bocchiaro CM, Greene RW, Feldman JL. Nicotinic excitation of rat hypoglossal motoneurons. Neuroscience 115: 861-870, 2002.
10. Changeux JP, Devillers-Thiery A, Chemouilli P. Acetylcholine receptor: an allosteric protein. Science 225: 1335-1345, 1984.
11. Colquhoun D, Sakmann B. From muscle endplate to brain synapses: a short history of synapses and agonist-activated ion channels. Neuron 20: 381-387, 1998.
12. Covernton PJ, Connolly JG. Multiple components in the agonist concentration-response relationships of neuronal nicotinic acetylcholine receptors. J Neurosci Methods 96: 63-70, 2000.
13. Di Angelantonio S, Nistri A. Calibration of agonist concentrations applied by pressure pulses or via rapid solution exchanger. J Neurosci Methods 110: 155-161, 2001.
14. Dwyer JB, Broide RS, Leslie FM. Nicotine and brain development. Birth Defects Res C Embryo Today 84: 30-44, 2008.
15. Eugenin J, Otarola M, Bravo E, Coddou C, Cerpa V, Reyes-Parada M, Llona I, von Bernhardi R. Prenatal to early postnatal nicotine exposure impairs central chemoreception and modifies breathing pattern in mouse neonates: a probable link to sudden infant death syndrome. J Neurosci 28: 13907-13917, 2008.
16. Fatt P, Katz B. An analysis of the end-plate potential recorded with an intracellular electrode. J Physiol 115: 320-370, 1951.
17. Fenster CP, Beckman ML, Parker JC, Sheffield EB, Whitworth TL, Quick MW, Lester RA. Regulation of alpha4beta2 nicotinic receptor desensitization by calcium and protein kinase C. Mol Pharmacol 55: 432-443, 1999.
18. Fenster CP, Rains MF, Noerager B, Quick MW, Lester RA. Influence of subunit composition on desensitization of neuronal acetylcholine receptors at low concentrations of nicotine. J Neurosci 17: 5747-5759, 1997.
19. Fewell JE, Smith FG. Perinatal nicotine exposure impairs ability of newborn rats to autoresuscitate from apnea during hypoxia. J Appl Physiol 85: 2066-2074, 1998.
20. Fewell JE, Smith FG, Ng VK. Prenatal exposure to nicotine impairs protective responses of rat pups to hypoxia in an age-dependent manner. Respir Physiol 127: 61-73, 2001a.
21. Fewell JE, Smith FG, Ng VK. Threshold levels of maternal nicotine impairing protective responses of newborn rats to intermittent hypoxia. J Appl Physiol 90: 1968-1976, 2001b.
22. Flores CM, Rogers SW, Pabreza LA, Wolfe BB, Kellar KJ. A subtype of nicotinic cholinergic receptor in rat brain is composed of alpha 4 and beta 2 subunits and is up-regulated by chronic nicotine treatment. Mol Pharmacol 41: 31-37, 1992.
23. Fregosi RF, Luo Z, Iizuka M. GABAA receptors mediate postnatal depression of respiratory frequency by barbiturates. Respir Physiol Neurobiol 140: 219-230, 2004.
24. Fregosi RF, Pilarski JQ. Prenatal nicotine exposure and development of nicotinic and fast amino acid-mediated neurotransmission in the control of breathing. Respir Physiol Neurobiol 164: 80-86, 2008.
25. Fregosi RF, Quan SF, Kaemingk KL, Morgan WJ, Goodwin JL, Cabrera R, Gmitro A. Sleep-disordered breathing, pharyngeal size and soft tissue anatomy in children. J Appl Physiol 95: 2030-2038, 2003.
26. Froen JF, Akre H, Stray-Pedersen B, Saugstad OD. Adverse effects of nicotine and interleukin-1beta on autoresuscitation after apnea in piglets: implications for sudden infant death syndrome. Pediatrics 105: E52, 2000.
27. Froen JF, Akre H, Stray-Pedersen B, Saugstad OD. Prolonged apneas and hypoxia mediated by nicotine and endotoxin in piglets. Biol Neonate 81: 119-125, 2002.
28. Fuller DD, Williams JS, Janssen PL, Fregosi RF. Effect of co-activation of tongue protrudor and retractor muscles on tongue movements and pharyngeal airflow mechanics in the rat. J Physiol 519: 601-613, 1999.
29. Funk GD, Smith JC, Feldman JL. Generation and transmission of respiratory oscillations in medullary slices: role of excitatory amino acids. J Neurophysiol 70: 1497-1515, 1993.
30. Galzi JL, Changeux JP. Neuronal nicotinic receptors: molecular organization and regulations. Neuropharmacology 34: 563-582, 1995.
31. Gentry CL, Lukas RJ. Regulation of nicotinic acetylcholine receptor numbers and function by chronic nicotine exposure. Curr Drug Targets CNS Neurol Disord 1: 359-385, 2002.
32. Giniatullin R, Nistri A, Yakel JL. Desensitization of nicotinic ACh receptors: shaping cholinergic signaling. Trends Neurosci 28: 371-378, 2005.
33. 2.JNeurophysiol 97:93-101,2007.
34. Hafstrom O, Milerad J, Asokan N, Poole SD, Sundell HW. Nicotine delays arousal during hypoxemia in lambs. Pediatr Res 47: 646-652, 2000.
35. Hafstrom O, Milerad J, Sandberg KL, Sundell HW. Cardiorespiratory effects of nicotine exposure during development. Respir Physiol Neurobiol 149: 325-341, 2005.
36. Hafstrom O, Milerad J, Sundell HW. Altered breathing pattern after prenatal nicotine exposure in the young lamb. Am J Respir Crit Care Med 166: 92-97, 2002a.
37. Hafstrom O, Milerad J, Sundell HW. Prenatal nicotine exposure blunts the cardiorespiratory response to hypoxia in lambs. Am J Respir Crit Care Med 166: 1544-1549, 2002b.
38. Huang YH, Brown AR, Costy-Bennett S, Luo Z, Fregosi RF. Influence of prenatal nicotine exposure on postnatal development of breathing pattern. Respir Physiol Neurobiol 143: 1-8, 2004a.
39. Huang YH, Brown AR, Cross SJ, Cruz J, Rice A, Jaiswal S, Fregosi RF. Influence of prenatal nicotine exposure on development of the ventilatory response to hypoxia and hypercapnia in neonatal rats. J Appl Physiol 109: 149-158, 2010.
40. Huang ZG, Griffioen KJ, Wang X, Dergacheva O, Kamendi H, Gorini C, Bouairi E, Mendelowitz D. Differential control of central cardiorespiratory interactions by hypercapnia and the effect of prenatal nicotine. J Neurosci 26: 21-29, 2006.
41. Huang ZG, Wang X, Evans C, Gold A, Bouairi E, Mendelowitz D. Prenatal nicotine exposure alters the types of nicotinic receptors that facilitate excitatory inputs to cardiac vagal neurons. J Neurophysiol 92: 2548-2554, 2004b.
42. Huganir RL, Greengard P. Regulation of neurotransmitter receptor desensitization by protein phosphorylation. Neuron 5: 555-567, 1990.
43. Kamendi HW, Cheng Q, Dergacheva O, Gorini C, Jameson HS, Wang X, McIntosh JM, Mendelowitz D. Abolishment of serotonergic neurotransmission to cardiac vagal neurons during and after hypoxia and hypercapnia with prenatal nicotine exposure. J Neurophysiol 101: 1141-1150, 2009.
44. Katz B, Thesleff S. A study of the desensitization produced by acetylcholine at the motor end-plate. J Physiol 138: 63-80, 1957.
45. Kinney HC, Richerson GB, Dymecki SM, Darnall RA, Nattie EE. The brainstem and serotonin in the sudden infant death syndrome. Annu Rev Pathol 4: 517-550, 2009.
46. Langley JN. On the contraction of muscle, chiefly in relation to the presence of "receptive" substances: Part I. J Physiol 36: 347-384, 1907.
47. Lester RA, Dani JA. Acetylcholine receptor desensitization induced by nicotine in rat medial habenula neurons. J Neurophysiol 74: 195-206, 1995.
48. Lewis KW, Bosque EM. Deficient hypoxia awakening response in infants of smoking mothers: possible relationship to sudden infant death syndrome. J Pediatr 127: 691-699, 1995.
49. Lukas RJ. Effects of chronic nicotinic ligand exposure on functional activity of nicotinic acetylcholine receptors expressed by cells of the PC12 rat pheochromocytoma or the TE671/RD human clonal line. J Neurochem 56: 1134-1145, 1991.
50. Luo Z, McMullen NT, Costy-Bennett S, Fregosi RF. Prenatal nicotine exposure alters glycinergic and GABAergic control of respiratory frequency in the neonatal rat brainstem-spinal cord preparation. Respir Physiol Neurobiol 157: 226-234, 2007.
51. Marks MJ, Grady SR, Collins AC. Downregulation of nicotine receptor function after chronic nicotine infusion. J Pharmacol Exp Ther 266: 1268-1276,1993.
52. Marubio LM, del Mar Arroyo-Jimenez M, Cordero-Erausquin M, Lena C, Le Novere N, de Kerchove d'Exaerde A, Huchet M, Damaj MI, Changeux JP. Reduced antinociception in mice lacking neuronal nicotinic receptor subunits. Nature 398: 805-810, 1999.
53. Miledi R. Intracellular calcium and desensitization of acetylcholine receptors. Proc R Soc Lond B Biol Sci 209: 447-452, 1980.
54. Neff RA, Simmens SJ, Evans C, Mendelowitz D. Prenatal nicotine exposure alters central cardiorespiratory responses to hypoxia in rats: implications for sudden infant death syndrome. J Neurosci 24: 9261-9268, 2004.
55. Papke RL, Meyer E, Nutter T, Uteshev VV. alpha7 receptor-selective agonists and modes of alpha7 receptor activation. Eur J Pharmacol 393: 179-195, 2000.
56. Paradiso K, Brehm P. Long-term desensitization of nicotinic acetylcholine receptors is regulated via protein kinase A-mediated phosphorylation. J Neurosci 18: 9227-9237, 1998.
57. Paradiso KG, Steinbach JH. Nicotine is highly effective at producing desensitization of rat alpha4beta2 neuronal nicotinic receptors. J Physiol 553: 857-871, 2003.
58. Peng X, Gerzanich V, Anand R, Wang F, Lindstrom J. Chronic nicotine treatment up-regulates alpha3 and alpha7 acetylcholine receptor subtypes expressed by the human neuroblastoma cell line SH-SY5Y. Mol Pharmacol 51: 776-784, 1997.
59. Peng X, Gerzanich V, Anand R, Whiting PJ, Lindstrom J. Nicotine- induced increase in neural nicotinic receptor results from a decrease in the rate of receptor turnover. Mol Pharmacol 46: 523-530, 1994.
60. Picciotto MR, Zoli M, Lena C, Bessis A, Lallemand Y, Le Novere N, Vincent P, Pich EM, Brulet P, Changeux JP. Abnormal avoidance learning in mice lacking functional high-affinity nicotine receptor in the brain. Nature 374: 65-67, 1995.
61. Pilarski JQ, Fregosi RF. Prenatal nicotine exposure alters medullary nicotinic and AMPA-mediated control of respiratory frequency in vitro. Respir Physiol Neurobiol 169: 1-10, 2009.
62. Pilarski JQ, Wakefield HE, Fuglevand AJ, Levine RB, Fregosi RF. Developmental nicotine exposure alters neurotransmission and excitability in hypoglossal motoneurons. J Neurophysiol 105: 423-433, 2010.
63. Quick MW, Lester RA. Desensitization of neuronal nicotinic receptors. J Neurobiol 53: 457-478, 2002.
64. 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 22: 2723-2734, 2005.
65. Rekling JC, Feldman JL. PreBotzinger complex and pacemaker neurons: hypothesized site and kernel for respiratory rhythm generation. Annu Rev Physiol 60: 385-405, 1998.
66. Robinson DM, Peebles KC, Kwok H, Adams BM, Clarke LL, Woollard GA, Funk GD. Prenatal nicotine exposure increases apnoea and reduces nicotinic potentiation of hypoglossal inspiratory output in mice. J Physiol 538: 957-973, 2002.
67. Rowell PP, Wonnacott S. Evidence for functional activity of up-regulated nicotine binding sites in rat striatal synaptosomes. J Neurochem 55: 2105-2110,1990.
68. Schoepfer R, Whiting P, Esch F, Blacher R, Shimasaki S, Lindstrom J. cDNA clones coding for the structural subunit of a chicken brain nicotinic acetylcholine receptor. Neuron 1: 241-248, 1988.
69. Shao XM, Feldman JL. Pharmacology of nicotinic receptors in preBotzinger complex that mediate modulation of respiratory pattern. J Neurophysiol 88: 1851-1858, 2002.
70. Shen JX, Yakel JL. Nicotinic acetylcholine receptor-mediated calcium signaling in the nervous system. Acta Pharmacol Sin 30: 673-680, 2009.
71. Slotkin TA, Lappi SE, McCook EC, Lorber BA, Seidler FJ. Loss of neonatal hypoxia tolerance after prenatal nicotine exposure: implications for sudden infant death syndrome. Brain Res Bull 38: 69-75, 1995.
72. Smith JC, Ellenberger HH, Ballanyi K, Richter DW, Feldman JL. PreBotzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science 254: 726-729, 1991.
73. Sokolova E, Matteoni C, Nistri A. Desensitization of neuronal nicotinic receptors of human neuroblastoma SH-SY5Y cells during short or long exposure to nicotine. Br J Pharmacol 146: 1087-1095, 2005.
74. St-John WM, Leiter JC. Maternal nicotine depresses eupneic ventilation of neonatal rats. Neurosci Lett 267: 206-208, 1999.
75. Tan W, Pagliardini S, Yang P, Janczewski WA, Feldman JL. Projections of preBotzinger complex neurons in adult rats. J Comp Neurol 518: 1862-1878, 2010.
76. Toubas PL, Duke JC, McCaffree MA, Mattice CD, Bendell D, Orr WC. Effects of maternal smoking and caffeine habits on infantile apnea: a retrospective study. Pediatrics 78: 159-163, 1986.
77. Tsunoyama K, Gojobori T. Evolution of nicotinic acetylcholine receptor subunits. Mol Biol Evol 15: 518-527, 1998.
78. Vallejo YF, Buisson B, Bertrand D, Green WN. Chronic nicotine exposure upregulates nicotinic receptors by a novel mechanism. J Neurosci 25: 5563-5572, 2005.
79. Whiting P, Esch F, Shimasaki S, Lindstrom J. Neuronal nicotinic acetylcholine receptor beta-subunit is coded for by the cDNA clone alpha 4. FEBS Lett 219: 459-463, 1987.
80. Wooltorton JR, Pidoplichko VI, Broide RS, Dani JA. Differential desensitization and distribution of nicotinic acetylcholine receptor subtypes in midbrain dopamine areas. J Neurosci 23: 3176-3185, 2003.
81. Wu J, Liu Q, Yu K, Hu J, Kuo YP, Segerberg M, St John PA, Lukas RJ. Roles of nicotinic acetylcholine receptor beta subunits in function of human alpha4-containing nicotinic receptors. J Physiol 576: 103-118, 2006.
82. Yu ZJ, Wecker L. Chronic nicotine administration differentially affects neurotransmitter release from rat striatal slices. J Neurochem 63: 186-194, 1994.
83. Zaninetti M, Tribollet E, Bertrand D, Raggenbass M. Presence of functional neuronal nicotinic acetylcholine receptors in brainstem motoneurons of the rat. Eur J Neurosci 11: 2737-2748, 1999.