Skip to main content

Advertisement

SpringerLink
Log in

Gene expression profiling of midbrain dopamine neurons upon gestational nicotine exposure

  • Original Article
  • Published:
Medical & Biological Engineering & Computing Aims and scope Submit manuscript

Abstract

Maternal smoking during pregnancy is associated with low birth weight, increased risk of stillbirth, conduct disorder, attention-deficit/hyperactivity disorder and neurocognitive deficits. Ventral tegmental area dopamine (DA) neurons in the mesocorticolimbic pathway were suggested to play a critical role in these pathological mechanisms induced by nicotine. Nicotine-mediated changes in genetic expression during pregnancy are of great interest for current researchers. We used patch clamp methods to identify and harvest DA and non-DA neurons separately and assayed them using oligonucleotide arrays to elucidate the alterations in gene expressions in these cells upon gestational nicotine exposure. Microarray analysis identified a set of 135 genes as significantly differentially expressed between DA and non-DA neurons. Some of the genes were found to be related to neurological disease pathways, such as Alzheimer’s disease, Parkinson’s disease and Huntington’s disease. Significantly up-/down-regulated genes found in DA neurons were mostly related to G-protein-coupled protein receptor signaling and developmental processes. These alterations in gene expressions may explain, partially at least, the possible pathological mechanisms for the diseases induced by maternal smoking.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Alcaro A, Huber R, Panksepp J (2007) Behavioral functions of the mesolimbic dopaminergic system: an affective neuroethological perspective. Brain Res Rev 56:283–321. doi:10.1016/j.brainresrev.2007.07.014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Bardy AH, Seppala T, Lillsunde P, Kataja JM, Koskela P, Pikkarainen J, Hiilesmaa VK (1993) Objectively measured tobacco exposure during pregnancy—neonatal effects and relation to maternal smoking. Br J Obstet Gynaecol 100:721–726. doi:10.1111/j.1471-0528.1993.tb14262.x

    Article  CAS  PubMed  Google Scholar 

  3. Betarbet R, Sherer TB, MacKenzie G, Garcia-Osuna M, Panov AV, Greenamyre JT (2000) Chronic systemic pesticide exposure reproduces features of Parkinson’s disease. Nat Neurosci 3:1301–1306

    Article  CAS  PubMed  Google Scholar 

  4. Bourre JM, Francois M, Youyou A, Dumont O, Piciotti M, Pascal G, Durand G (1989) The effects of dietary alpha-linolenic acid on the composition of nerve membranes, enzymatic-activity, amplitude of electrophysiological parameters, resistance to poisons and performance of learning-tasks in rats. J Nutr 119:1880–1892

    CAS  PubMed  Google Scholar 

  5. Brischoux F, Fellmann D, Risold PY (2001) Ontogenetic development of the diencephalic MCH neurons: a hypothalamic ‘MCH area’ hypothesis. Eur J Neurosci 13:1733–1744. doi:10.1046/j.0953-816x.2001.01552.x

    Article  CAS  PubMed  Google Scholar 

  6. Britt JP, McGehee DS (2008) Presynaptic opioid and nicotinic receptor modulation of dopamine overflow in the nucleus accumbens. J Neurosci 28:1672–1681. doi:10.1523/jneurosci.4275-07.2008

    Article  CAS  PubMed  Google Scholar 

  7. Brouillet E, Conde F, Beal MF, Hantraye P (1999) Replicating Huntington’s disease phenotype in experimental animals. Prog Neurobiol 59:427–468. doi:10.1016/s0301-0082(99)00005-2

    Article  CAS  PubMed  Google Scholar 

  8. Browne CJ, Sharma N, Waters KA, Machaalani R (2010) The effects of nicotine on the alpha-7 and beta-2 nicotinic acetylcholine receptor subunits in the developing piglet brainstem. Int J Dev Neurosci 28:1–7. doi:10.1016/j.ijdevneu.2009.10.005

    Article  CAS  PubMed  Google Scholar 

  9. Buchberger A, Howard MJ, Proctor M, Bycroft M (2001) The UBX domain: a widespread ubiquitin-like module. J Mol Biol 307:17–24. doi:10.1006/jmbi.2000.4462

    Article  CAS  PubMed  Google Scholar 

  10. Buka SL, Shenassa ED, Niaura R (2003) Elevated risk of tobacco dependence among offspring of mothers who smoked during pregnancy: a 30-year prospective study. Am J Psychiatry 160:1978–1984. doi:10.1176/appi.ajp.160.11.1978

    Article  PubMed  Google Scholar 

  11. Cajigas IJ, Will T, Schuman EM (2010) Protein homeostasis and synaptic plasticity. EMBO J 29:2746–2752. doi:10.1038/emboj.2010.173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Carpenter AC, Saborido TP, Stanwood GD (2012) Development of hyperactivity and anxiety responses in dopamine transporter-deficient mice. Dev Neurosci 34:250–257. doi:10.1159/000336824

    Article  CAS  PubMed  Google Scholar 

  13. Chandrasekaran K, Hatanpaa K, Rapoport SI, Brady DR (1997) Decreased expression of nuclear and mitochondrial DNA-encoded genes of oxidative phosphorylation in association neocortex in Alzheimer disease. Brain Res Mol Brain Res 44:99–104

    Article  CAS  PubMed  Google Scholar 

  14. Chen H, Parker SL, Matta SG, Sharp BM (2005) Gestational nicotine exposure reduces nicotinic cholinergic receptor (nAChR) expression in dopaminergic brain regions of adolescent rats. Eur J Neurosci 22:380–388. doi:10.1111/j.1460-9568.2005.04229.x

    Article  PubMed  Google Scholar 

  15. Christianson JC, Green WN (2004) Regulation of nicotinic receptor expression by the ubiquitin–proteasome system. EMBO J 23:4156–4165. doi:10.1038/sj.emboj.7600436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Cornelius MD, Day NL (2009) Developmental consequences of prenatal tobacco exposure. Curr Opin Neurol 22:121–125. doi:10.1097/WCO.0b013e328326f6dc

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. DiAntonio A, Hicke L (2004) Ubiquitin-dependent regulation of the synapse. Annu Rev Neurosci 27:223–246. doi:10.1146/annurev.neuro.27.070203.144317

    Article  CAS  PubMed  Google Scholar 

  18. Ding S, Wei W, Zhou F-M (2011) Molecular and functional differences in voltage-activated sodium currents between GABA projection neurons and dopamine neurons in the substantia nigra. J Neurophysiol 106:3019–3034. doi:10.1152/jn.00305.2011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Ekblad M, Korkeila J, Parkkola R, Lapinleimu H, Haataja L, Lehtonen L, Grp PS (2010) Maternal smoking during pregnancy and regional brain volumes in preterm infants. J Pediatr 156:185-U140. doi:10.1016/j.jpeds.2009.07.061

    Article  CAS  Google Scholar 

  20. Enslen M, Milon H, Malnoe A (1991) Effect of low intake of n-3 fatty-acids during development on brain phospholipid fatty-acid composition and exploratory-behavior in rats. Lipids 26:203–208. doi:10.1007/bf02543972

    Article  CAS  PubMed  Google Scholar 

  21. Frances H, Monier C, Clement M, Lecorsier A, Debray M, Bourre JM (1996) Effect of dietary alpha-linolenic acid deficiency on habituation. Life Sci 58:1805–1816. doi:10.1016/0024-3205(96)00164-6

    Article  CAS  PubMed  Google Scholar 

  22. Fried PA, Watkinson B, Gray R (1992) A follow-up-study of attentional behavior in 6-year-old children exposed prenatally to marijuana, cigarettes, and alcohol. Neurotoxicol Teratol 14:299–311. doi:10.1016/0892-0362(92)90036-a

    Article  CAS  PubMed  Google Scholar 

  23. Fukuyama R, Hatanpaa K, Rapoport SI, Chandrasekaran K (1996) Gene expression of ND4, a subunit of complex I of oxidative phosphorylation in mitochondria, is decreased in temporal cortex of brains of Alzheimer’s disease patients. Brain Res 713:290–293. doi:10.1016/0006-8993(95)01517-5

    Article  CAS  PubMed  Google Scholar 

  24. Gaimarri A, Moretti M, Riganti L, Zanardi A, Clementi F, Gotti C (2007) Regulation of neuronal nicotinic receptor traffic and expression. Brain Res Rev 55:134–143. doi:10.1016/j.brainresrev.2007.02.005

    Article  CAS  PubMed  Google Scholar 

  25. Gainetdinov RR, Caron MG (2000) An animal model of attention deficit hyperactivity disorder. Mol Med Today 6:43–44. doi:10.1016/s1357-4310(99)01616-0

    Article  CAS  PubMed  Google Scholar 

  26. Garrido R, Mattson MP, Hennig B, Toborek M (2001) Nicotine protects against arachidonic-acid-induced caspase activation, cytochrome c release and apoptosis of cultured spinal cord neurons. J Neurochem 76:1395–1403. doi:10.1046/j.1471-4159.2001.00135.x

    Article  CAS  PubMed  Google Scholar 

  27. Giros B, Caron MG (1993) Molecular characterization of the dopamine transporter. Trends Pharmacol Sci 14:43–49. doi:10.1016/0165-6147(93)90029-j

    Article  CAS  PubMed  Google Scholar 

  28. Gizer IR, Ficks C, Waldman ID (2009) Candidate gene studies of ADHD: a meta-analytic review. Hum Genet 126:51–90. doi:10.1007/s00439-009-0694-x

    Article  CAS  PubMed  Google Scholar 

  29. Haglund K, Dikic I (2005) Ubiquitylation and cell signaling. EMBO J 24:3353–3359. doi:10.1038/sj.emboj.7600808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Harrod SB, Lacy RT, Zhu J, Hughes BA, Perna MK, Brown RW (2011) Gestational IV nicotine produces elevated brain-derived neurotrophic factor in the mesocorticolimbic dopamine system of adolescent rat offspring. Synapse 65:1382–1392. doi:10.1002/syn.20975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Herrmann M, King K, Weitzman M (2008) Prenatal tobacco smoke and postnatal secondhand smoke exposure and child neurodevelopment. Curr Opin Pediatr 20:184–190. doi:10.1097/MOP.0b013e3282f56165

    Article  PubMed  Google Scholar 

  32. Hill SY, Lowers L, Locke-Wellman J, Shen SA (2000) Maternal smoking and drinking during pregnancy and the risk for child and adolescent psychiatric disorders. J Stud Alcohol 61:661–668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Hnasko TS, Chuhma N, Zhang H, Goh GY, Sulzer D, Palmiter RD, Rayport S, Edwards RH (2010) Vesicular glutamate transport promotes dopamine storage and glutamate corelease in vivo. Neuron 65:643–656. doi:10.1016/j.neuron.2010.02.012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Huang DW, Sherman BT, Lempicki RA (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37:1–13. doi:10.1093/nar/gkn923

    Article  CAS  Google Scholar 

  35. Huang DW, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44–57. doi:10.1038/nprot.2008.211

    Article  CAS  Google Scholar 

  36. Hubert GW, Jones DC, Moffett MC, Rogge G, Kuhar MJ (2008) CART peptides as modulators of dopamine and psychostimulants and interactions with the mesolimbic dopaminergic system. Biochem Pharmacol 75:57–62. doi:10.1016/j.bcp.2007.07.028

    Article  CAS  PubMed  Google Scholar 

  37. Jaworski JN, Jones DC (2006) The role of CART in the reward/reinforcing properties of psychostimulants. Peptides 27:1993–2004. doi:10.1016/j.peptides.2006.03.034

    Article  CAS  PubMed  Google Scholar 

  38. Jentsch S, Rumpf S (2007) Cdc48 (p97): a ‘molecular gearbox’ in the ubiquitin pathway? Trends Biochem Sci 32:6–11. doi:10.1016/j.tibs.2006.11.005

    Article  CAS  PubMed  Google Scholar 

  39. Johansen EB, Killeen PR, Russell VA, Tripp G, Wickens JR, Tannock R, Williams J, Sagvolden T (2009) Origins of altered reinforcement effects in ADHD. Behav Brain Funct. doi:10.1186/1744-9081-5-7

    PubMed  PubMed Central  Google Scholar 

  40. Jones S, Kornblum JL, Kauer JA (2000) Amphetamine blocks long-term synaptic depression in the ventral tegmental area. J Neurosci 20:5575–5580

    CAS  PubMed  Google Scholar 

  41. Kahn RS, Khoury J, Nichols WC, Lanphear BP (2003) Role of dopamine transporter genotype and maternal prenatal smoking in childhood hyperactive-impulsive, inattentive, and oppositional behaviors. J Pediatr 143:104–110. doi:10.1016/s0022-3476(03)00208-7

    Article  PubMed  Google Scholar 

  42. Kane VB, Fu YT, Matta SG, Sharp BM (2004) Gestational nicotine exposure attenuates nicotine-stimulated dopamine release in the nucleus accumbens shell of adolescent Lewis rats. J Pharmacol Exp Ther 308:521–528. doi:10.1124/jpet.103.059899

    Article  CAS  PubMed  Google Scholar 

  43. Kauer JA, Malenka RC (2007) Synaptic plasticity and addiction. Nat Rev Neurosci 8:844–858. doi:10.1038/nrn2234

    Article  CAS  PubMed  Google Scholar 

  44. Keller JN, Hanni KB, Markesbery WR (2000) Impaired proteasome function in Alzheimer’s disease. J Neurochem 75:436–439. doi:10.1046/j.1471-4159.2000.0750436.x

    Article  CAS  PubMed  Google Scholar 

  45. Kheradpezhouh M, Shavali S, Ebadi M (2003) Salsolinol causing parkinsonism activates endoplasmic reticulum-stress signaling pathways in human dopaminergic SK-N-SH cells. Neurosignals 12:315–324. doi:10.1159/000075314

    Article  CAS  PubMed  Google Scholar 

  46. Kim J, Moody JP, Edgerly CK, Bordiuk OL, Cormier K, Smith K, Beal MF, Ferrante RJ (2010) Mitochondrial loss, dysfunction and altered dynamics in Huntington’s disease. Hum Mol Genet 19:3919–3935. doi:10.1093/hmg/ddq306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Kimmel HL, Gong WH, Dall Vechia S, Hunter RG, Kuhar MJ (2000) Intra-ventral tegmental area injection of rat cocaine and amphetamine-regulated transcript peptide 55-102 induces locomotor activity and promotes conditioned place preference. J Pharmacol Exp Ther 294:784–792

    CAS  PubMed  Google Scholar 

  48. Klann E, Antion MD, Banko JL, Hou LF (2004) Synaptic plasticity and translation initiation. Learn Mem 11:365–372. doi:10.1101/lm.79004

    Article  PubMed  Google Scholar 

  49. Klink R, d’Exaerde AD, Zoli M, Changeux JP (2001) Molecular and physiological diversity of nicotinic acetylcholine receptors in the midbrain dopaminergic nuclei. J Neurosci 21:1452–1463

    CAS  PubMed  Google Scholar 

  50. Kopito RR, Ron D (2000) Conformational disease. Nat Cell Biol 2:E207–E209. doi:10.1038/35041139

    Article  CAS  PubMed  Google Scholar 

  51. Korotkova TM, Ponomarenko AA, Brown RE, Haas HL (2004) Functional diversity of ventral midbrain dopamine and GABAergic neurons. Mol Neurobiol 29:243–259. doi:10.1385/mn:29:3:243

    Article  CAS  PubMed  Google Scholar 

  52. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645. doi:10.1101/gr.092759.109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Kurtoglu S, Gunes T, Koklu E, Bastug O, Canoz O, Kula M, Bastug F, Gunes I (2007) Influence of maternal nicotine exposure on neonatal rat bone: protective effect of pentoxifylline. Exp Biol Med 232:398–405

    CAS  Google Scholar 

  54. Langston JW, Ballard P, Tetrud JW, Irwin I (1983) Chronic parkinsonism in humans due to a product of meperidine-analog synthesis. Science 219:979–980. doi:10.1126/science.6823561

    Article  CAS  PubMed  Google Scholar 

  55. Lauro C, Di Angelantonio S, Cipriani R, Sobrero F, Antonilli L, Brusadin V, Ragozzino D, Limatola C (2008) Activity of adenosine receptors type 1 is required for CX(3)CL1-mediated neuroprotection and neuromodulation in hippocampal neurons. J Immunol 180:7590–7596

    Article  CAS  PubMed  Google Scholar 

  56. le Blanc LMP, van Lieshout AWT, Adema GJ, van Riel P, Verbeek MM, Radstake T (2006) CXCL16 is elevated in the cerebrospinal fluid versus serum and in inflammatory conditions with suspected and proved central nervous system involvement. Neurosci Lett 397:145–148. doi:10.1016/j.neulet.2005.12.029

    Article  PubMed  CAS  Google Scholar 

  57. Li LB, Chen NH, Ramamoorthy S, Chi LM, Cui XN, Wang LJC, Reith MEA (2004) The role of N-glycosylation in function and surface trafficking of the human dopamine transporter. J Biol Chem 279:21012–21020. doi:10.1074/jbc.M311972200

    Article  CAS  PubMed  Google Scholar 

  58. Li Q, Lu G, Antonio GE, Mak YT, Rudd JA, Fan M, Yew DT (2007) The usefulness of spontaneously hypertensive rat to model attention-deficit/hyperactivity disorder (ADHD) may be explained by the differential expression of dopamine-related genes in the brain. Neurochem Int 50:848–857. doi:10.1016/j.neuint.2007.02.005

    Article  CAS  PubMed  Google Scholar 

  59. Lim DK, Park SH, Choi WJ (2000) Subacute nicotine exposure in cultured cerebellar cells increased the release and uptake of glutamate. Arch Pharmacal Res 23:488–494. doi:10.1007/bf02976578

    Article  CAS  Google Scholar 

  60. Lim KL, Tan JMM (2007) Role of the ubiquitin proteasome system in Parkinson’s disease. BMC Biochem. doi:10.1186/1471-2091-8-S1-S13

    PubMed  PubMed Central  Google Scholar 

  61. Lopez-Hidalgo M, Salgado-Puga K, Alvarado-Martinez R, Cristina Medina A, Prado-Alcala RA, Garcia-Colunga J (2012) Nicotine uses neuron-glia communication to enhance hippocampal synaptic transmission and long-term memory. Plos One. doi:10.1371/journal.pone.0049998

    PubMed  PubMed Central  Google Scholar 

  62. Louis JCM (1996) Methods of preventing neuron degeneration and promoting neuron regeneration. Amgen

  63. Luck W, Nau H (1984) Nicotine and cotinine concentrations in serum and milk of nursing smokers. Br J Clin Pharmacol 18:9–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Margolis EB, Lock H, Hjelmstad GO, Fields HL (2006) The ventral tegmental area revisited: is there an electrophysiological marker for dopaminergic neurons? J Physiol Lond 577:907–924. doi:10.1113/jphysiol.2006.117069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Meyer H (2012) p97 complexes as signal integration hubs. BMC Biol. doi:10.1186/1741-7007-10-48

    PubMed  Google Scholar 

  66. Navarro HA, Seidler FJ, Whitmore WL, Slotkin TA (1988) Prenatal exposure to nicotine via maternal infusions-effects on development of catecholamine systems. J Pharmacol Exp Ther 244:940–944

    CAS  PubMed  Google Scholar 

  67. Neuman RJ, Lobos E, Reich W, Henderson CA, Sun L-W, Todd RD (2007) Prenatal smoking exposure and dopaminergic genotypes interact to cause a severe ADHD subtype. Biol Psychiatry 61:1320–1328. doi:10.1016/j.biopsych.2006.08.049

    Article  CAS  PubMed  Google Scholar 

  68. Nisell M, Marcus M, Nomikos GG, Svensson TH (1997) Differential effects of acute and chronic nicotine on dopamine output in the core and shell of the rat nucleus accumbens. J Neural Transm 104:1–10. doi:10.1007/bf01271290

    Article  CAS  PubMed  Google Scholar 

  69. Nishizaki T, Nomura T, Matsuoka T, Enikolopov G, Sumikawa K (1999) Arachidonic acid induces a long-lasting facilitation of hippocampal synaptic transmission by modulating PKC activity and nicotinic ACh receptors. Mol Brain Res 69:263–272. doi:10.1016/s0169-328x(99)00117-5

    Article  CAS  PubMed  Google Scholar 

  70. Owens SD, Innis SM (1999) Docosahexaenoic and arachidonic acid prevent a decrease in dopaminergic and serotoninergic neurotransmitters in frontal cortex caused by a linoleic and alpha-linolenic acid deficient diet in formula-fed piglets. J Nutr 129:2088–2093

    Google Scholar 

  71. Parker WD, Parks J, Filley CM, Kleinschmidtdemasters BK (1994) Electron-transport chain defects in Alzheimers-disease brain. Neurology 44:1090–1096

    Article  PubMed  Google Scholar 

  72. Parker WD, Swerdlow RH (1998) Mitochondrial dysfunction in idiopathic Parkinson disease. Am J Hum Genet 62:758–762. doi:10.1086/301812

    Article  PubMed  PubMed Central  Google Scholar 

  73. Pauly JR, Slotkin TA (2008) Maternal tobacco smoking, nicotine replacement and neurobehavioural development. Acta Paediatr 97:1331–1337. doi:10.1111/j.1651-2227.2008.00852.x

    Article  PubMed  Google Scholar 

  74. Pierce RC, Kumaresan V (2006) The mesolimbic dopamine system: the final common pathway for the reinforcing effect of drugs of abuse? Neurosci Biobehav Rev 30:215–238. doi:10.1016/j.neubiorev.2005.04.016

    Article  CAS  PubMed  Google Scholar 

  75. Rezvani K, Teng Y, Shim D, De Biasi M (2007) Nicotine regulates multiple synaptic proteins by inhibiting proteasomal activity. J Neurosci 27:10508–10519. doi:10.1523/jneurosci.3353-07.2007

    Article  CAS  PubMed  Google Scholar 

  76. Ribary U, Lichtensteiger W (1989) Effects of acute and chronic prenatal nicotine treatment on central catecholamine systems of male and female rat fetuses and offspring. J Pharmacol Exp Ther 248:786–792

    CAS  PubMed  Google Scholar 

  77. Richardson SA, Tizabi Y (1994) Hyperactivity in the offspring of nicotine-treated rats—role of the mesolimbic and nigrostriatal dopaminergic pathways. Pharmacol Biochem Behav 47:331–337. doi:10.1016/0091-3057(94)90018-3

    Article  CAS  PubMed  Google Scholar 

  78. Rosito M, Deflorio C, Limatola C, Trettel F (2012) CXCL16 orchestrates adenosine A(3) receptor and MCP-1/CCL2 activity to protect neurons from excitotoxic cell death in the CNS. J Neurosci 32:3154–3163. doi:10.1523/jneurosci.4046-11.2012

    Article  CAS  PubMed  Google Scholar 

  79. Roy TS, Sabherwal U (1998) Effects of gestational nicotine exposure on hippocampal morphology. Neurotoxicol Teratol 20:465–473. doi:10.1016/s0892-0362(97)00137-2

    Article  CAS  PubMed  Google Scholar 

  80. Roy TS, Seidler FJ, Slotkin TA (2002) Prenatal nicotine exposure evokes alterations of cell structure in hippocampus and somatosensory cortex. J Pharmacol Exp Ther 300:124–133. doi:10.1124/jpet.300.1.124

    Article  CAS  PubMed  Google Scholar 

  81. Roza SJ, Verburg BO, Jaddoe VWV, Hofman A, Mackenbach JP, Steegers EAP, Witteman JCM, Verhulst FC, Tiemeier H (2007) Effects of maternal smoking in pregnancy on prenatal brain development. The Generation R Study. Eur J Neurosci 25:611–617. doi:10.1111/j.1460-9568.2007.05393.x

    Article  PubMed  Google Scholar 

  82. Salihu HM, Wilson RE, Alio AP, Kirby RS (2008) Advanced maternal age and risk of antepartum and intrapartum stillbirth. J Obstet Gynaecol Res 34:843–850. doi:10.1111/j.1447-0756.2008.00855.x

    Article  PubMed  Google Scholar 

  83. Sastry PS (1985) Lipids of nervous-tissue-composition and metabolism. Prog Lipid Res 24:69–176. doi:10.1016/0163-7827(85)90011-6

    Article  CAS  PubMed  Google Scholar 

  84. Schneider T, Ilott N, Brolese G, Bizarro L, Asherson PJE, Stolerman IP (2011) Prenatal exposure to nicotine impairs performance of the 5-choice serial reaction time task in adult rats. Neuropsychopharmacology 36:1114–1125. doi:10.1038/npp.2010.249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Schuberth C, Buchberger A (2008) UBX domain proteins: major regulators of the AAA ATPase Cdc48/p97. Cell Mol Life Sci 65:2360–2371. doi:10.1007/s00018-008-8072-8

    Article  CAS  PubMed  Google Scholar 

  86. Selkoe DJ (2003) Folding proteins in fatal ways. Nature 426:900–904. doi:10.1038/nature02264

    Article  CAS  PubMed  Google Scholar 

  87. Sershen H, Mason MF, Reith MEA, Hashim A, Lajtha A (1986) Effect of amphetamine on 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) neurotoxicity in mice. Neuropharmacology 25:927–930. doi:10.1016/0028-3908(86)90022-5

    Article  CAS  PubMed  Google Scholar 

  88. Slotkin TA, Cho H, Whitmore WL (1987) Effects of prenatal nicotine exposure on neuronal development—selective actions on central and peripheral catecholaminergic pathways. Brain Res Bull 18:601–611. doi:10.1016/0361-9230(87)90130-4

    Article  CAS  PubMed  Google Scholar 

  89. Soto-Otero R, Mendez-Alvarez E, Hermida-Ameijeiras A, Lopez-Real AM, Labandeira-Garcia JL (2002) Effects of (−)-nicotine and (−)-cotinine on 6-hydroxydopamine-induced oxidative stress and neurotoxicity: relevance for Parkinson’s disease. Biochem Pharmacol 64:125–135. doi:10.1016/s0006-2952(02)01070-5

    Article  CAS  PubMed  Google Scholar 

  90. Sprecher H, Luthria DL, Mohammed BS, Baykousheva SP (1995) Reevaluation of the pathways for the biosynthesis of polyunsaturated fatty acids. J Lipid Res 36:2471–2477

    CAS  PubMed  Google Scholar 

  91. Sutton MA, Schuman EM (2006) Dendritic protein synthesis, synaptic plasticity, and memory. Cell 127:49–58. doi:10.1016/j.cell.2006.09.014

    Article  CAS  PubMed  Google Scholar 

  92. Swan GE, Lessov-Schlaggar CN (2007) The effects of tobacco smoke and nicotine on cognition and the brain. Neuropsychol Rev 17:259–273. doi:10.1007/s11065-007-9035-9

    Article  PubMed  Google Scholar 

  93. Thapar A, van den Bree M, Fowler T, Langley K, Whittinger N (2006) Predictors of antisocial behaviour in children with attention deficit hyperactivity disorder. Eur Child Adolesc Psychiatry 15:118–125. doi:10.1007/s00787-006-0511-1

    Article  PubMed  Google Scholar 

  94. Ungless MA, Whistler JL, Malenka RC, Bonci A (2001) Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature 411:583–587. doi:10.1038/35079077

    Article  CAS  PubMed  Google Scholar 

  95. Vanbockstaele EJ, Pickel VM (1995) GABA-containing neurons in the ventral tegmental area project to the nucleus-accumbens in rat-brain. Brain Res 682:215–221. doi:10.1016/0006-8993(95)00334-m

    Article  CAS  Google Scholar 

  96. Vlahakis SR, Villasis-Keever A, Gomez T, Vanegas M, Vlahakis N, Paya CV (2002) G protein-coupled chemokine receptors induce both survival and apoptotic signaling pathways. J Immunol 169:5546–5554

    Article  CAS  PubMed  Google Scholar 

  97. Wakschlag LS, Lahey BB, Loeber R, Green SM, Gordon RA, Leventhal BL (1997) Maternal smoking during pregnancy and the risk of conduct disorder in boys. Arch Gen Psychiatry 54:670–676

    Article  CAS  PubMed  Google Scholar 

  98. Wang J, Duncan D, Shi Z, Zhang B (2013) WEB-based GEne SeT AnaLysis Toolkit (WebGestalt): update 2013. Nucleic Acids Res 41:W77–W83. doi:10.1093/nar/gkt439

    Article  PubMed  PubMed Central  Google Scholar 

  99. Ward SG, Westwick J (1998) Chemokines: understanding their role in T-lymphocyte biology. Biochem J 333:457–470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Weissman MM, Warner V, Wickramaratne PJ, Kandel DB (1999) Maternal smoking during pregnancy and psychopathology in offspring followed to adulthood. J Am Acad Child Adolesc Psychiatry 38:892–899. doi:10.1097/00004583-199907000-00020

    Article  CAS  PubMed  Google Scholar 

  101. White SR, Lauring B (2007) AAA+ ATPases: achieving diversity of function with conserved machinery. Traffic 8:1657–1667. doi:10.1111/j.1600-0854.2007.00642.x

    Article  CAS  PubMed  Google Scholar 

  102. Wise RA (1985) The anhedonia hypothesis—mark-III. Behav Brain Sci 8:178–184

    Article  Google Scholar 

  103. Yamamoto BK, Novotney S (1998) Regulation of extracellular dopamine by the norepinephrine transporter. J Neurochem 71:274–280

    Article  CAS  PubMed  Google Scholar 

  104. Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP (2002) Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res. doi:10.1093/nar/30.4.e15

    Google Scholar 

  105. Yi JJ, Ehlers MD (2007) Emerging roles for ubiquitin and protein degradation in neuronal function. Pharmacol Rev 59:14–39. doi:10.1124/pr.59.1.4

    Article  CAS  PubMed  Google Scholar 

  106. Zhang B, Kirov S, Snoddy J (2005) WebGestalt: an integrated system for exploring gene sets in various biological contexts. Nucleic Acids Res 33:W741–W748. doi:10.1093/nar/gki475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Zhang H, Li S, Wang M, Vukusic B, Pristupa ZB, Liu F (2009) Regulation of dopamine transporter activity by carboxypeptidase E. Molecular Brain. doi:10.1186/1756-6606-2-10

    Google Scholar 

  108. Zhang TA, Placzek AN, Dani JA (2010) In vitro identification and electrophysiological characterization of dopamine neurons in the ventral tegmental area. Neuropharmacology 59:431–436. doi:10.1016/j.neuropharm.2010.06.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Zhu J, Apparsundaram S, Dwoskin LP (2009) Nicotinic receptor activation increases H-3 dopamine uptake and cell surface expression of dopamine transporters in rat prefrontal cortex. J Pharmacol Exp Ther 328:931–939. doi:10.1124/jpet.108.147025

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biomedical Engineering, University of Houston, SERC Building, 3605 Cullen Blvd, Houston, TX, 77204, USA

    Pınar Kanlikilicer, Die Zhang, Andrei Dragomir, Yasemin M. Akay & Metin Akay

Authors
  1. Pınar Kanlikilicer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Die Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andrei Dragomir
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yasemin M. Akay
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Metin Akay
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Metin Akay.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Fig. 1

Timeline for the sample collections and presentation of samples used in this study. (PDF 98 kb)

Supplementary Fig. 2

Heatmap displaying the expression fold changes of the 135 differentially expressed genes in DA vs non-DA neurons. (PDF 93 kb)

Supplementary Fig. 3

Compact diagram of working flow of WebGestalt program. (PDF 76 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kanlikilicer, P., Zhang, D., Dragomir, A. et al. Gene expression profiling of midbrain dopamine neurons upon gestational nicotine exposure. Med Biol Eng Comput 55, 467–482 (2017). https://doi.org/10.1007/s11517-016-1531-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11517-016-1531-8

Keywords

Search

Navigation