Effects of sex and chronic neonatal nicotine treatment on Na2+/K+/Cl- co-transporter 1, K+/Cl- co-transporter 2, brain-derived neurotrophic factor, NMDA receptor subunit 2A and NMDA receptor subunit 2B mRNA expression in the postnatal rat hippocampus

Neuroscience

Volumn 225, Issue , 2012, Pages 105-117

  Damborsky, J C ^a   Winzer Serhan, U H ^a  

^a TEXAS A AND M UNIVERSITY SYSTEM   (United States)

Author keywords

Development; GABAergic; In situ hybridization; NAChR; Nicotinic; NMDA

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; NICOTINE; NICOTINIC RECEPTOR; POTASSIUM CHLORIDE COTRANSPORTER; POTASSIUM CHLORIDE COTRANSPORTER 2; SODIUM POTASSIUM CHLORIDE COTRANSPORTER; SODIUM POTASSIUM CHLORIDE COTRANSPORTER 1; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; EXCITATORY JUNCTION POTENTIAL; FEMALE; HIPPOCAMPUS; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERINATAL DRUG EXPOSURE; PERINATAL PERIOD; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SENSITIVITY ANALYSIS; SEX DIFFERENCE; SIGNAL TRANSDUCTION; SYNAPTOGENESIS;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BRAIN-DERIVED NEUROTROPHIC FACTOR; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIPPOCAMPUS; MALE; NICOTINE; NICOTINIC AGONISTS; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; RNA, MESSENGER; SEX CHARACTERISTICS; SODIUM-POTASSIUM-CHLORIDE SYMPORTERS; TIME FACTORS;

EID: 84867129637     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.09.002     Document Type: Article

References (73)

1. Adams C.E., Broide R.S., Chen Y., Winzer-Serhan U.H., Henderson T.A., Leslie F.M., Freedman R. Development of the alpha7 nicotinic cholinergic receptor in rat hippocampal formation. Brain Res Dev Brain Res 2002, 139:175-187.
2. Aguado F., Carmona M.A., Pozas E., Aguilo A., Martinez-Guijarro F.J., Alcantara S., Borrell V., Yuste R., Ibanez C.F., Soriano E. BDNF regulates spontaneous correlated activity at early developmental stages by increasing synaptogenesis and expression of the K+/Cl- co-transporter KCC2. Development 2003, 130:1267-1280.
3. Alkondon M., Pereira E.F., Albuquerque E.X. Alpha-bungarotoxin- and methyllycaconitine-sensitive nicotinic receptors mediate fast synaptic transmission in interneurons of rat hippocampal slices. Brain Res 1998, 810:257-263.
4. Alkondon M., Pereira E.F., Eisenberg H.M., Albuquerque E.X. Choline and selective antagonists identify two subtypes of nicotinic acetylcholine receptors that modulate GABA release from CA1 interneurons in rat hippocampal slices. J Neurosci 1999, 19:2693-2705.
5. Aramakis V.B., Hsieh C.Y., Leslie F.M., Metherate R. A critical period for nicotine-induced disruption of synaptic development in rat auditory cortex. J Neurosci 2000, 20:6106-6116.
6. Bale T.L., Baram T.Z., Brown A.S., Goldstein J.M., Insel T.R., McCarthy M.M., Nemeroff C.B., Reyes T.M., Simerly R.B., Susser E.S., Nestler E.J. Early life programming and neurodevelopmental disorders. Biol Psychiatry 2010, 68:314-319.
7. Barria A., Malinow R. Subunit-specific NMDA receptor trafficking to synapses. Neuron 2002, 35:345-353.
8. Bellone C., Nicoll R.A. Rapid bidirectional switching of synaptic NMDA receptors. Neuron 2007, 55:779-785.
9. Ben-Ari Y. Excitatory actions of gaba during development: the nature of the nurture. Nat Rev Neurosci 2002, 3:728-739.
10. Berchtold N.C., Oliff H.S., Isackson P., Cotman C.W. Hippocampal BDNF mRNA shows a diurnal regulation, primarily in the exon III transcript. Brain Res Mol Brain Res 1999, 71:11-22.
11. Berninger B., Marty S., Zafra F., da Penha Berzaghi M., Thoenen H., Lindholm D. GABAergic stimulation switches from enhancing to repressing BDNF expression in rat hippocampal neurons during maturation in vitro. Development 1995, 121:2327-2335.
12. Bray J.G., Mynlieff M. Influx of calcium through L-type calcium channels in early postnatal regulation of chloride transporters in the rat hippocampus. Dev Neurobiol 2009, 69:885-896. erratum 897-912.
13. Cancedda L., Fiumelli H., Chen K., Poo M.M. Excitatory GABA action is essential for morphological maturation of cortical neurons in vivo. J Neurosci 2007, 27:5224-5235.
14. Cull-Candy S., Brickley S., Farrant M. NMDA receptor subunits: diversity, development and disease. Curr Opin Neurobiol 2001, 11:327-335.
15. Damborsky J.C., Griffith W.H., Winzer-Serhan U.H. Chronic neonatal nicotine exposure increases excitation in the young adult rat hippocampus in a sex-dependent manner. Brain Res 2012, 1430:8-17.
16. Dobbing J., Sands J. Comparative aspects of the brain growth spurt. Early Hum Dev 1979, 3:79-83.
17. Durand G.M., Konnerth A. Long-term potentiation as a mechanism of functional synapse induction in the developing hippocampus. J Physiol Paris 1996, 90:313-315.
18. Dwyer J.B., Broide R.S., Leslie F.M. Nicotine and brain development. Birth Defects Res C Embryo Today 2008, 84:30-44.
19. Fiala J.C., Feinberg M., Popov V., Harris K.M. Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J Neurosci 1998, 18:8900-8911.
20. Frazier C.J., Rollins Y.D., Breese C.R., Leonard S., Freedman R., Dunwiddie T.V. Acetylcholine activates an alpha-bungarotoxin-sensitive nicotinic current in rat hippocampal interneurons, but not pyramidal cells. J Neurosci 1998, 18:1187-1195.
21. Galanopoulou A.S. Dissociated gender-specific effects of recurrent seizures on GABA signaling in CA1 pyramidal neurons: role of GABA(A) receptors. J Neurosci 2008, 28:1557-1567.
22. Galanopoulou A.S. Sexually dimorphic expression of KCC2 and GABA function. Epilepsy Res 2008, 80:99-113.
23. Ganguly K., Schinder A.F., Wong S.T., Poo M. GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell 2001, 105:521-532.
24. Goebel D.J., Poosch M.S. NMDA receptor subunit gene expression in the rat brain: a quantitative analysis of endogenous mRNA levels of NR1Com, NR2A, NR2B, NR2C, NR2D and NR3A. Brain Res Mol Brain Res 1999, 69:164-170.
25. Gotti C., Zoli M., Clementi F. Brain nicotinic acetylcholine receptors: native subtypes and their relevance. Trends Pharmacol Sci 2006, 27:482-491.
26. 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.
27. Hsia A.Y., Malenka R.C., Nicoll R.A. Development of excitatory circuitry in the hippocampus. J Neurophysiol 1998, 79:2013-2024.
28. Hsieh C.Y., Leslie F.M., Metherate R. Nicotine exposure during a postnatal critical period alters NR2A and NR2B mRNA expression in rat auditory forebrain. Brain Res Dev Brain Res 2002, 133:19-25.
29. Huang L.Z., Hsiao S.H., Trzeciakowski J., Frye G.D., Winzer-Serhan U.H. Chronic nicotine induces growth retardation in neonatal rat pups. Life Sci 2006, 78:1483-1493.
30. Huang L.Z., Abbott L.C., Winzer-Serhan U.H. Effects of chronic neonatal nicotine exposure on nicotinic acetylcholine receptor binding, cell death and morphology in hippocampus and cerebellum. Neuroscience 2007, 146:1854-1868.
31. Huang L.Z., Liu X., Griffith W.H., Winzer-Serhan U.H. Chronic neonatal nicotine increases anxiety but does not impair cognition in adult rats. Behav Neurosci 2007, 121:1342-1352.
32. Isaac J.T., Nicoll R.A., Malenka R.C. Evidence for silent synapses: implications for the expression of LTP. Neuron 1995, 15:427-434.
33. Ishii T., Moriyoshi K., Sugihara H., Sakurada K., Kadotani H., Yokoi M., Akazawa C., Shigemoto R., Mizuno N., Masu M., et al. Molecular characterization of the family of the N-methyl-d-aspartate receptor subunits. J Biol Chem 1993, 268:2836-2843.
34. Jones S., Yakel J.L. Functional nicotinic ACh receptors on interneurones in the rat hippocampus. J Physiol 1997, 504(Pt. 3):603-610.
35. Lee H., Chen C.X., Liu Y.J., Aizenman E., Kandler K. KCC2 expression in immature rat cortical neurons is sufficient to switch the polarity of GABA responses. Eur J Neurosci 2005, 21:2593-2599.
36. Liu Z., Neff R.A., Berg D.K. Sequential interplay of nicotinic and GABAergic signaling guides neuronal development. Science 2006, 314:1610-1613.
37. Lu J., Karadsheh M., Delpire E. Developmental regulation of the neuronal-specific isoform of K-Cl cotransporter KCC2 in postnatal rat brains. J Neurobiol 1999, 39:558-568.
38. Luck W., Nau H., Hansen R., Steldinger R. Extent of nicotine and cotinine transfer to the human fetus, placenta and amniotic fluid of smoking mothers. Dev Pharmacol Ther 1985, 8:384-395.
39. Maggi L., Sher E., Cherubini E. Regulation of GABA release by nicotinic acetylcholine receptors in the neonatal rat hippocampus. J Physiol 2001, 536:89-100.
40. Maggi L., Le Magueresse C., Changeux J.P., Cherubini E. Nicotine activates immature " silent" connections in the developing hippocampus. Proc Natl Acad Sci U S A 2003, 100:2059-2064.
41. Maggi L., Sola E., Minneci F., Le Magueresse C., Changeux J.P., Cherubini E. Persistent decrease in synaptic efficacy induced by nicotine at Schaffer collateral-CA1 synapses in the immature rat hippocampus. J Physiol 2004, 559:863-874.
42. Matta J.A., Ashby M.C., Sanz-Clemente A., Roche K.W., Isaac J.T. MGluR5 and NMDA receptors drive the experience- and activity-dependent NMDA receptor NR2B to NR2A subunit switch. Neuron 2011, 70:339-351.
43. Monyer H., Burnashev N., Laurie D.J., Sakmann B., Seeburg P.H. Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 1994, 12:529-540.
44. Murrin L.C., Ferrer J.R., Zeng W.Y., Haley N.J. Nicotine administration to rats: methodological considerations. Life Sci 1987, 40:1699-1708.
45. Nunez J.L., McCarthy M.M. Evidence for an extended duration of GABA-mediated excitation in the developing male versus female hippocampus. Dev Neurobiol 2007, 67:1879-1890.
46. Obrietan K., van den Pol A.N. GABA neurotransmission in the hypothalamus: developmental reversal from Ca2+ elevating to depressing. J Neurosci 1995, 15:5065-5077.
47. Obrietan K., Gao X.B., Van Den Pol A.N. Excitatory actions of GABA increase BDNF expression via a MAPK-CREB-dependent mechanism - a positive feedback circuit in developing neurons. J Neurophysiol 2002, 88:1005-1015.
48. Payne J.A., Rivera C., Voipio J., Kaila K. Cation-chloride co-transporters in neuronal communication, development and trauma. Trends Neurosci 2003, 26:199-206.
49. Pfeffer C.K., Stein V., Keating D.J., Maier H., Rinke I., Rudhard Y., Hentschke M., Rune G.M., Jentsch T.J., Hubner C.A. NKCC1-dependent GABAergic excitation drives synaptic network maturation during early hippocampal development. J Neurosci 2009, 29:3419-3430.
50. Plotkin M.D., Snyder E.Y., Hebert S.C., Delpire E. Expression of the Na-K-2Cl cotransporter is developmentally regulated in postnatal rat brains: a possible mechanism underlying GABA's excitatory role in immature brain. J Neurobiol 1997, 33:781-795.
51. Radcliffe K.A., Dani J.A. Nicotinic stimulation produces multiple forms of increased glutamatergic synaptic transmission. J Neurosci 1998, 18:7075-7083.
52. Radcliffe K.A., Fisher J.L., Gray R., Dani J.A. Nicotinic modulation of glutamate and GABA synaptic transmission of hippocampal neurons. Ann N Y Acad Sci 1999, 868:591-610.
53. Represa A., Ben-Ari Y. Trophic actions of GABA on neuronal development. Trends Neurosci 2005, 28:278-283.
54. Rivera C., Voipio J., Payne J.A., Ruusuvuori E., Lahtinen H., Lamsa K., Pirvola U., Saarma M., Kaila K. The K+/Cl- co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 1999, 397:251-255.
55. SAMHSA (2010) Results from the 2009 National Survey on Drug Use and Health: Volume I. Summary of National Findings. (Office of Applied Studies, N.S.H.-A., HHS Publication No. SMA 10-4856Findings, ed). Rockville, MD.
56. Sargent P.B. The diversity of neuronal nicotinic acetylcholine receptors. Annu Rev Neurosci 1993, 16:403-443.
57. Son J.H., Winzer-Serhan U.H. Postnatal expression of alpha2 nicotinic acetylcholine receptor subunit mRNA in developing cortex and hippocampus. J Chem Neuroanat 2006, 32:179-190.
58. Son J.H., Winzer-Serhan U.H. Chronic neonatal nicotine exposure increases mRNA expression of neurotrophic factors in the postnatal rat hippocampus. Brain Res 2009, 1278:1-14.
59. Stein V., Hermans-Borgmeyer I., Jentsch T.J., Hubner C.A. Expression of the KCl cotransporter KCC2 parallels neuronal maturation and the emergence of low intracellular chloride. J Comp Neurol 2004, 468:57-64.
60. 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.
61. Tyzio R., Represa A., Jorquera I., Ben-Ari Y., Gozlan H., Aniksztejn L. The establishment of GABAergic and glutamatergic synapses on CA1 pyramidal neurons is sequential and correlates with the development of the apical dendrite. J Neurosci 1999, 19:10372-10382.
62. Vaglenova J., Birru S., Pandiella N.M., Breese C.R. An assessment of the long-term developmental and behavioral teratogenicity of prenatal nicotine exposure. Behav Brain Res 2004, 150:159-170.
63. Vaglenova J., Parameshwaran K., Suppiramaniam V., Breese C.R., Pandiella N., Birru S. Long-lasting teratogenic effects of nicotine on cognition: gender specificity and role of AMPA receptor function. Neurobiol Learn Mem 2008, 90:527-536.
64. Wang C., Shimizu-Okabe C., Watanabe K., Okabe A., Matsuzaki H., Ogawa T., Mori N., Fukuda A., Sato K. Developmental changes in KCC1, KCC2, and NKCC1 mRNA expressions in the rat brain. Brain Res Dev Brain Res 2002, 139:59-66.
65. Wang H., Davila-Garcia M.I., Yarl W., Gondre-Lewis M.C. Gestational nicotine exposure regulates expression of AMPA and NMDA receptors and their signaling apparatus in developing and adult rat hippocampus. Neuroscience 2011, 188:168-181.
66. Wardle R.A., Poo M.M. Brain-derived neurotrophic factor modulation of GABAergic synapses by postsynaptic regulation of chloride transport. J Neurosci 2003, 23:8722-8732.
67. Weissman M.M., Warner V., Wickramaratne P.J., Kandel D.B. Maternal smoking during pregnancy and psychopathology in offspring followed to adulthood. J Am Acad Child Adolesc Psychiatry 1999, 38:892-899.
68. Winzer-Serhan U.H. Long-term consequences of maternal smoking and developmental chronic nicotine exposure. Front Biosci 2008, 13:636-649.
69. Winzer-Serhan U.H., Leslie F.M. Expression of alpha5 nicotinic acetylcholine receptor subunit mRNA during hippocampal and cortical development. J Comp Neurol 2005, 481:19-30.
70. Winzer-Serhan U.H., Broide R.S., Chen Y., Leslie F.M. Highly sensitive radioactive in situ hybridization using full length hydrolyzed riboprobes to detect alpha 2 adrenoceptor subtype mRNAs in adult and developing rat brain. Brain Res Brain Res Protoc 1999, 3:229-241.
71. Yamada M.K., Nakanishi K., Ohba S., Nakamura T., Ikegaya Y., Nishiyama N., Matsuki N. Brain-derived neurotrophic factor promotes the maturation of GABAergic mechanisms in cultured hippocampal neurons. J Neurosci 2002, 22:7580-7585.
72. Yamada J., Okabe A., Toyoda H., Kilb W., Luhmann H.J., Fukuda A. Cl- uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1. J Physiol 2004, 557:829-841.
73. Zhong J., Carrozza D.P., Williams K., Pritchett D.B., Molinoff P.B. Expression of mRNAs encoding subunits of the NMDA receptor in developing rat brain. J Neurochem 1995, 64:531-539.