Skip to main content

Advertisement

SpringerLink
Log in

Ventral Tegmental Transcriptome Response to Intermittent Nicotine Treatment and Withdrawal in BALB/cJ, C57BL/6ByJ, and Quasi-Congenic RQI Mice

  • Original Paper
  • Published:
Neurochemical Research Aims and scope Submit manuscript

Abstract

The aim of this study was to identify neurochemical pathways and candidate genes involved in adaptation to nicotine treatment and withdrawal. Locomotor sensitization was assessed in a nicotine challenge test after exposure to intermittent nicotine treatment and withdrawal. About 24 h after the challenge test the ventral tegmentum of the mesencephalon was dissected and processed using oligonucleotide microarrays with 22,690 probe sets (Affymetrix 430A 2.0). Quasi-congenic RQI, and donor BALB/cJ mice developed significant locomotor sensitization, while sensitization was not significant in the background partner, C57BL/6By. Comparing saline treated controls of C57BL/6ByJ and BALB/cJ by a rigorous statistical microarray analysis method we identified 238 differentially expressed transcripts. Quasi-congenic strains B6.Cb4i5-α4/Vad and B6.Ib5i7-β25A/Vad significantly differed from the background strain in 11 and 11 transcripts, respectively. Identification of several cis- and trans-regulated genes indicates that further work with quasi-congenic strains can quickly lead to mapping of Quantitative Trait Loci for nicotine susceptibility because donor chromosome regions have been mapped in quasi-congenic strains. Nicotine treatment significantly altered the abundance of 41, 29, 54, and 14 ventral tegmental transcripts in strains C57BL/6ByJ, BALB/cJ, B6.Cb4i5-α4/Vad, and B6.Ib5i7-β25A/Vad, respectively. Although transcript sets overlapped to some extent, each strain showed a distinct profile of nicotine sensitive genes, indicating genetic effects on nicotine-induced gene expression. Nicotine-responsive genes were related to processes including regulation of signal transduction, intracellular protein transport, proteasomal ubiquitin-dependent protein catabolism, and neuropeptide signaling pathway. Our results suggest that while there are common regulatory mechanisms across inbred strains, even relatively small differences in genetic constitution can significantly affect transcriptome response to nicotine.

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
Fig. 6

Similar content being viewed by others

References

  1. Celik E, Uzbay IT, Karakas S (2005) Caffeine and amphetamine produce cross-sensitization to nicotine-induced locomotor activity in mice. Prog Neuropsychopharmacol Biol Psychiatry [Epub ahead of print]

  2. Saito M, O’brien D, Kovacs KM, Wang R, Zavadil J, Vadasz C (2005) Nicotine-induced sensitization in mice: changes in locomotor activity and mesencephalic gene expression. Neurochem Res 30:1027–1035

    Article  PubMed  CAS  Google Scholar 

  3. Benwell ME, Balfour DJ (1992) The effects of acute and repeated nicotine treatment on nucleus accumbens dopamine and locomotor activity. Br J Pharmacol 105:849–856

    PubMed  CAS  Google Scholar 

  4. Shim I, Javaid JI, Wirtshafter D, Jang SY, Shin KH, Lee HJ, Chung YC, Chun BG (2001) Nicotine-induced behavioral sensitization is associated with extracellular dopamine release and expression of c-Fos in the striatum and nucleus accumbens of the rat. Behav Brain Res 121:137–147

    Article  PubMed  CAS  Google Scholar 

  5. Clarke PB, Fu DS, Jakubovic A, Fibiger HC (1988) Evidence that mesolimbic dopaminergic activation underlies the locomotor stimulant action of nicotine in rats. J Pharmacol Exp Ther 246:701–708

    PubMed  CAS  Google Scholar 

  6. Le Foll B, Diaz J, Sokoloff P (2003) Increased dopamine D3 receptor expression accompanying behavioral sensitization to nicotine in rats. Synapse 47:176–183

    Article  PubMed  CAS  Google Scholar 

  7. Mexal S, Frank M, Berger R, Adams CE, Ross RG, Freedman R, Leonard S (2005) Differential modulation of gene expression in the NMDA postsynaptic density of schizophrenic and control smokers. Brain Res Mol Brain Res 139:317–332

    Article  PubMed  CAS  Google Scholar 

  8. Zhang S, Day IN, Ye S (2001) Microarray analysis of nicotine-induced changes in gene expression in endothelial cells. Physiol Genomics 5:187–192

    PubMed  CAS  Google Scholar 

  9. Belluardo N, Olsson PA, Mudo G, Sommer WH, Amato G, Fuxe K (2005) Transcription factor gene expression profiling after acute intermittent nicotine treatment in the rat cerebral cortex. Neuroscience 133:787–796

    Article  PubMed  CAS  Google Scholar 

  10. Kane JK, Konu O, Ma JZ, Li MD (2004) Nicotine coregulates multiple pathways involved in protein modification/degradation in rat brain. Brain Res Mol Brain Res 132:181–191

    Article  PubMed  CAS  Google Scholar 

  11. Li MD, Kane JK, Wang J, Ma JZ (2004) Time-dependent changes in transcriptional profiles within five rat brain regions in response to nicotine treatment. Brain Res Mol Brain Res 132:168–180

    Article  PubMed  CAS  Google Scholar 

  12. Hu D, Cao K, Peterson-Wakeman R, Wang R (2002) Altered profile of gene expression in rat hearts induced by chronic nicotine consumption. Biochem Biophys Res Commun 297:729–736

    Article  PubMed  CAS  Google Scholar 

  13. Konu O, Kane JK, Barrett T, Vawter MP, Chang R, Ma JZ, Donovan DM, Sharp B, Becker KG, Li MD (2001) Region-specific transcriptional response to chronic nicotine in rat brain. Brain Res 909:194–203

    Article  PubMed  CAS  Google Scholar 

  14. Thibault C, Hassan S, Miles M (2005) Using in vitro models for expression profiling studies on ethanol and drugs of abuse. Addict Biol 10:53–62

    Article  PubMed  CAS  Google Scholar 

  15. Konu O, Xu X, Ma JZ, Kane J, Wang J, Shi SJ, Li MD (2004) Application of a customized pathway-focused microarray for gene expression profiling of cellular homeostasis upon exposure to nicotine in PC12 cells. Brain Res Mol Brain Res 121:102–113

    Article  PubMed  CAS  Google Scholar 

  16. Dunckley T, Lukas RJ (2003) Nicotine modulates the expression of a diverse set of genes in the neuronal SH-SY5Y cell line. J Biol Chem 278:15633–15640

    Article  PubMed  CAS  Google Scholar 

  17. Vadasz C (1990) Development of congenic recombinant inbred neurological animal model lines. Mouse Genome 88:16–18

    Google Scholar 

  18. Vadasz C, Sziraki I, Murthy LR, Sasvari-Szekely M, Kabai P, Laszlovszky I, Fleischer A, Juhasz B, Zahorchak R (1994) Transfer of brain dopamine system-specific quantitative trait loci onto a C57BL/6ByJ background. Mamm Genome 5:735–737

    Article  PubMed  CAS  Google Scholar 

  19. Vadasz C, Sziraki I, Sasvari M, Kabai P, Laszlovszky I, Juhasz B, Zahorchak R (1996) Genomic characterization of two introgression strains (B6.Cb4i5) for the analysis of QTLs. Mamm Genome 7:545–548

    Article  PubMed  CAS  Google Scholar 

  20. Vadasz C, Sziraki I, Balla A, Lafrancois J, Mao R (1997) Recombinant QTL Introgression animal models serve as a novel tool for mapping dopamine-system genes. Am J Med Genet 74:584–585

    Google Scholar 

  21. Vadasz C, Sziraki I, Sasvari M, Kabai P, Murthy LR, Saito M, Laszlovszky I (1998) Analysis of the mesotelencephalic dopamine system by quantitative-trait locus introgression. Neurochem Res 23:1337–1354

    Article  PubMed  CAS  Google Scholar 

  22. Sershen H, Hashim A, Vadasz C (2002) Strain and sex differences in repeated ethanol treatment-induced motor activity in quasi-congenic mice. Genes Brain Behav 1:156–165

    Article  PubMed  CAS  Google Scholar 

  23. Vincent VA, Devoss JJ, Ryan HS, Murphy GM Jr (2002) Analysis of neuronal gene expression with laser capture microdissection. J Neurosci Res 69:578–586

    Article  PubMed  CAS  Google Scholar 

  24. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  25. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264

    Article  PubMed  Google Scholar 

  26. Hosack DA, Dennis G Jr, Sherman BT, Lane HC, Lempicki RA (2003) Identifying biological themes within lists of genes with EASE. Genome Biol 4:R70

    Article  PubMed  Google Scholar 

  27. Gygi SP, Rochon Y, Franza BR, Aebersold R (1999) Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 19:1720–1730

    PubMed  CAS  Google Scholar 

  28. Donelan MJ, Morfini G, Julyan R, Sommers S, Hays L, Kajio H, Briaud I, Easom RA, Molkentin JD, Brady ST, Rhodes CJ (2002) Ca2+-dependent dephosphorylation of kinesin heavy chain on beta-granules in pancreatic beta-cells. Implications for regulated beta-granule transport and insulin exocytosis. J Biol Chem 277:24232–24242

    Article  PubMed  CAS  Google Scholar 

  29. Cho GW, Kim MH, Chai YG, Gilmor ML, Levey AI, Hersh LB (2000) Phosphorylation of the rat vesicular acetylcholine transporter. J Biol Chem 275:19942–19948

    Article  PubMed  CAS  Google Scholar 

  30. Castell X, Cheviron N, Barnier JV, Diebler MF (2003) Exploring the regulation of the expression of ChAT and VAChT genes in NG108–15 cells: implication of PKA and PI3K signaling pathways. Neurochem Res 28:557–564

    Article  PubMed  CAS  Google Scholar 

  31. Li LY, Shih HM, Liu MY, Chen JY (2001) The cellular protein PRA1 modulates the anti-apoptotic activity of Epstein-Barr virus BHRF1, a homologue of Bcl-2, through direct interaction. J Biol Chem 276:27354–27362

    Article  PubMed  CAS  Google Scholar 

  32. Shibasaki F, Kondo E, Akagi T, Mckeon F (1997) Suppression of signalling through transcription factor NF-AT by interactions between calcineurin and Bcl-2. Nature 386:728–731

    Article  PubMed  CAS  Google Scholar 

  33. Berthier A, Lemaire-Ewing S, Prunet C, Montange T, Vejux A, Pais De Barros JP, Monier S, Gambert P, Lizard G, Neel D (2005) 7-Ketocholesterol-induced apoptosis. FEBS J 272:3093–3104

    Article  PubMed  CAS  Google Scholar 

  34. Macphail RC, Farmer JD, Jarema KA, Chernoff N (2005) Nicotine effects on the activity of mice exposed prenatally to the nicotinic agonist anatoxin-a. Neurotoxicol Teratol 27:593–598

    Article  PubMed  CAS  Google Scholar 

  35. Biala G (2003) Calcium channel antagonists suppress nicotine-induced place preference and locomotor sensitization in rodents. Pol J Pharmacol 55:327–335

    PubMed  CAS  Google Scholar 

  36. Ulusu U, Uzbay IT, Kayir H, Alici T, Karakas S (2005) Evidence for the role of nitric oxide in nicotine-induced locomotor sensitization in mice. Psychopharmacology (Berl) 178:500–504

    Article  CAS  Google Scholar 

  37. Yoo JH, Cho JH, Lee SY, Loh HH, Ho IK, Jang CG (2005) Reduced nNOS expression induced by repeated nicotine treatment in mu-opioid receptor knockout mice. Neurosci Lett 380:70–74

    Article  PubMed  CAS  Google Scholar 

  38. Yoo JH, Lee SY, Loh HH, Ho IK, Jang CG (2004) Loss of nicotine-induced behavioral sensitization in micro-opioid receptor knockout mice. Synapse 51:219–223

    Article  PubMed  CAS  Google Scholar 

  39. Vadasz C, Saito M, Gyetvai B, Mikics E, Vadasz C 2nd (2000) Scanning of five chromosomes for alcohol consumption loci. Alcohol 22:25–34

    Article  PubMed  CAS  Google Scholar 

  40. Balfour DJ, Benwell ME, Birrell CE, Kelly RJ, Al-Aloul M (1998) Sensitization of the mesoaccumbens dopamine response to nicotine. Pharmacol Biochem Behav 59:1021–1030

    Article  PubMed  CAS  Google Scholar 

  41. Balfour DJ (2004) The neurobiology of tobacco dependence: a preclinical perspective on the role of the dopamine projections to the nucleus accumbens [corrected]. Nicotine Tob Res 6:899–912

    Article  PubMed  CAS  Google Scholar 

  42. Bolanos CA, Neve RL, Nestler EJ (2005) Phospholipase C gamma in distinct regions of the ventral tegmental area differentially regulates morphine-induced locomotor activity. Synapse 56:166–169

    Article  PubMed  CAS  Google Scholar 

  43. Valjent E, Pascoli V, Svenningsson P, Paul S, Enslen H, Corvol JC, Stipanovich A, Caboche J, Lombroso PJ, Nairn AC, Greengard P, Herve D, Girault JA (2005) Regulation of a protein phosphatase cascade allows convergent dopamine and glutamate signals to activate ERK in the striatum. Proc Natl Acad Sci U S A 102:491–496

    Article  PubMed  CAS  Google Scholar 

  44. Buchwalter G, Gross C, Wasylyk B (2004) Ets ternary complex transcription factors. Gene 324:1–14

    Article  PubMed  CAS  Google Scholar 

  45. Nisell M, Nomikos GG, Chergui K, Grillner P, Svensson TH (1997) Chronic nicotine enhances basal and nicotine-induced Fos immunoreactivity preferentially in the medial prefrontal cortex of the rat. Neuropsychopharmacology 17:151–161

    Article  PubMed  CAS  Google Scholar 

  46. Harlan RE, Garcia MM (1998) Drugs of abuse and immediate-early genes in the forebrain. Mol Neurobiol 16:221–267

    PubMed  CAS  Google Scholar 

  47. Kane JK, Parker SL, Matta SG, Fu Y, Sharp BM, Li MD (2000) Nicotine up-regulates expression of orexin and its receptors in rat brain. Endocrinology 141:3623–3629

    Article  PubMed  CAS  Google Scholar 

  48. Li MD, Kane JK, Parker SL, Mcallen K, Matta SG, Sharp BM (2000) Nicotine administration enhances NPY expression in the rat hypothalamus. Brain Res 867:157–164

    Article  PubMed  CAS  Google Scholar 

  49. Ficklin MB, Zhao S, Feng G (2005) Ubiquilin-1 regulates nicotine-induced up-regulation of neuronal nicotinic acetylcholine receptors. J Biol Chem 280:34088–34095

    Article  PubMed  CAS  Google Scholar 

  50. Li MD, Konu O, Kane JK, Becker KG (2002) Microarray technology and its application on nicotine research. Mol Neurobiol 25:265–285

    Article  PubMed  CAS  Google Scholar 

  51. Saito M, Szakall I, Toth R, Kovacs KM, Oros M, Prasad VV, Blumenberg M, Vadasz C (2004) Mouse striatal transcriptome analysis: effects of oral self-administration of alcohol. Alcohol 32:223–241

    Article  PubMed  CAS  Google Scholar 

  52. Flores CM, Rogers SW, Pabreza LA, Wolfe BB, Kellar KJ (1992) 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

    PubMed  CAS  Google Scholar 

  53. Schwartz RD, Kellar KJ (1983) Nicotinic cholinergic receptor binding sites in the brain: regulation in vivo. Science 220:214–216

    Article  PubMed  CAS  Google Scholar 

  54. Marks MJ, Pauly JR, Gross SD, Deneris ES, Hermans-Borgmeyer I, Heinemann SF, Collins AC (1992) Nicotine binding and nicotinic receptor subunit RNA after chronic nicotine treatment. J Neurosci 12:2765–2784

    PubMed  CAS  Google Scholar 

  55. Christianson JC, Green WN (2004) Regulation of nicotinic receptor expression by the ubiquitin-proteasome system. Embo J 23:4156–4165

    Article  PubMed  CAS  Google Scholar 

  56. Kukkonen JP, Holmqvist T, Ammoun S, Akerman KE (2002) Functions of the orexinergic/hypocretinergic system. Am J Physiol Cell Physiol 283:C1567–C1591

    PubMed  CAS  Google Scholar 

  57. Sakurai T, Amemiya A, Ishii M, Matsuzaki I, Chemelli RM, Tanaka H, Williams SC, Richardson JA, Kozlowski GP, Wilson S, Arch JR, Buckingham RE, Haynes AC, Carr SA, Annan RS, Mcnulty DE, Liu WS, Terrett JA, Elshourbagy NA, Bergsma DJ, Yanagisawa M (1998) Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92:573–585

    Article  PubMed  CAS  Google Scholar 

  58. Bourgin P, Huitron-Resendiz S, Spier AD, Fabre V, Morte B, Criado JR, Sutcliffe JG, Henriksen SJ, De Lecea L (2000) Hypocretin-1 modulates rapid eye movement sleep through activation of locus coeruleus neurons. J Neurosci 20:7760–7765

    PubMed  CAS  Google Scholar 

  59. Harris GC, Wimmer M, Aston-Jones G (2005) A role for lateral hypothalamic orexin neurons in reward seeking. Nature 437:556–559

    Article  PubMed  CAS  Google Scholar 

  60. Sakurai T, Nagata R, Yamanaka A, Kawamura H, Tsujino N, Muraki Y, Kageyama H, Kunita S, Takahashi S, Goto K, Koyama Y, Shioda S, Yanagisawa M (2005) Input of orexin/hypocretin neurons revealed by a genetically encoded tracer in mice. Neuron 46:297–308

    Article  PubMed  CAS  Google Scholar 

  61. De Lecea L, Kilduff TS, Peyron C, Gao X, Foye PE, Danielson PE, Fukuhara C, Battenberg EL, Gautvik VT, Bartlett FS 2nd, Frankel WN, Van Den Pol AN, Bloom FE, Gautvik KM, Sutcliffe JG (1998) The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci U S A 95:322–327

    Article  PubMed  Google Scholar 

  62. Kane JK, Parker SL, Li MD (2001) Hypothalamic orexin-A binding sites are downregulated by chronic nicotine treatment in the rat. Neurosci Lett 298:1–4

    Article  PubMed  CAS  Google Scholar 

  63. Hokfelt T, Rehfeld JF, Skirboll L, Ivemark B, Goldstein M, Markey K (1980) Evidence for coexistence of dopamine and CCK in meso-limbic neurones. Nature 285:476–478

    Article  PubMed  CAS  Google Scholar 

  64. Tsujino N, Yamanaka A, Ichiki K, Muraki Y, Kilduff TS, Yagami K, Takahashi S, Goto K, Sakurai T (2005) Cholecystokinin activates orexin/hypocretin neurons through the cholecystokinin A receptor. J Neurosci 25:7459–7469

    Article  PubMed  CAS  Google Scholar 

  65. Takimoto T, Terayama H, Waga C, Okayama T, Ikeda K, Fukunishi I, Iwahashi K (2005) Cholecystokinin (CCK) and the CCKA receptor gene polymorphism, and smoking behavior. Psychiatry Res 133:123–128

    Article  PubMed  CAS  Google Scholar 

  66. Giniatullin R, Nistri A, Yakel JL (2005) Desensitization of nicotinic ACh receptors: shaping cholinergic signaling. Trends Neurosci 28:371–378

    Article  PubMed  CAS  Google Scholar 

  67. New HV, Mudge AW (1986) Calcitonin gene-related peptide regulates muscle acetylcholine receptor synthesis. Nature 323:809–811

    Article  PubMed  CAS  Google Scholar 

  68. Leff SE, Evans RM, Rosenfeld MG (1987) Splice commitment dictates neuron-specific alternative RNA processing in calcitonin/CGRP gene expression. Cell 48:517–524

    Article  PubMed  CAS  Google Scholar 

  69. Di Angelantonio S, Giniatullin R, Costa V, Sokolova E, Nistri A (2003) Modulation of neuronal nicotinic receptor function by the neuropeptides CGRP and substance P on autonomic nerve cells. Br J Pharmacol 139:1061–1073

    Article  PubMed  CAS  Google Scholar 

  70. Mulle C, Benoit P, Pinset C, Roa M, Changeux JP (1988) Calcitonin gene-related peptide enhances the rate of desensitization of the nicotinic acetylcholine receptor in cultured mouse muscle cells. Proc Natl Acad Sci U S A 85:5728–5732

    Article  PubMed  CAS  Google Scholar 

  71. Giniatullin R, Di Angelantonio S, Marchetti C, Sokolova E, Khiroug L, Nistri A (1999) Calcitonin gene-related peptide rapidly downregulates nicotinic receptor function and slowly raises intracellular Ca2+ in rat chromaffin cells in vitro. J Neurosci 19:2945–2953

    PubMed  CAS  Google Scholar 

  72. Jinno S, Hua XY, Yaksh TL (1994) Nicotine and acetylcholine induce release of calcitonin gene-related peptide from rat trachea. J Appl Physiol 76:1651–1656

    PubMed  CAS  Google Scholar 

  73. Dussor GO, Leong AS, Gracia NB, Kilo S, Price TJ, Hargreaves KM, Flores CM (2003) Potentiation of evoked calcitonin gene-related peptide release from oral mucosa: a potential basis for the pro-inflammatory effects of nicotine. Eur J Neurosci 18:2515–2526

    Article  PubMed  Google Scholar 

  74. Orazzo C, Pieribone VA, Ceccatelli S, Terenius L, Hokfelt T (1993) CGRP-like immunoreactivity in A11 dopamine neurons projecting to the spinal cord and a note on CGRP-CCK cross-reactivity. Brain Res 600:39–48

    Article  PubMed  CAS  Google Scholar 

  75. Hokfelt T, Arvidsson U, Ceccatelli S, Cortes R, Cullheim S, Dagerlind A, Johnson H, Orazzo C, Piehl F, Pieribone V, Et Al (1992) Calcitonin gene-related peptide in the brain, spinal cord, and some peripheral systems. Ann N Y Acad Sci 657:119–134

    Article  PubMed  CAS  Google Scholar 

  76. Salmon AM, Damaj I, Sekine S, Picciotto MR, Marubio L, Changeux JP (1999) Modulation of morphine analgesia in alphaCGRP mutant mice. Neuroreport 10:849–854

    Article  PubMed  CAS  Google Scholar 

  77. Salmon AM, Evrard A, Damaj I, Changeux JP (2004) Reduction of withdrawal signs after chronic nicotine exposure of alpha-calcitonin gene-related peptide knock-out mice. Neurosci Lett 360:73–76

    Article  PubMed  CAS  Google Scholar 

  78. Fischer JA, Muff R, Born W (2002) Functional relevance of G-protein-coupled-receptor-associated proteins, exemplified by receptor-activity-modifying proteins (RAMPs). Biochem Soc Trans 30:455–460

    Article  PubMed  CAS  Google Scholar 

  79. Miret JJ, Rakhilina L, Silverman L, Oehlen B (2002) Functional expression of heteromeric calcitonin gene-related peptide and adrenomedullin receptors in yeast. J Biol Chem 277:6881–6887

    Article  PubMed  CAS  Google Scholar 

  80. Bomberger JM, Parameswaran N, Hall CS, Aiyar N, Spielman WS (2005) Novel function for receptor activity-modifying proteins (RAMPs) in post-endocytic receptor trafficking. J Biol Chem 280:9297–9307

    Article  PubMed  CAS  Google Scholar 

  81. Jansen RC, Nap JP (2001) Genetical genomics: the added value from segregation. Trends Genet 17:388–391

    Article  PubMed  CAS  Google Scholar 

  82. Brem RB, Yvert G, Clinton R, Kruglyak L (2002) Genetic dissection of transcriptional regulation in budding yeast. Science 296:752–755

    Article  PubMed  CAS  Google Scholar 

  83. Brem RB, Kruglyak L (2005) The landscape of genetic complexity across 5,700 gene expression traits in yeast. Proc Natl Acad Sci U S A 102:1572–1577

    Article  PubMed  CAS  Google Scholar 

  84. Yvert G, Brem RB, Whittle J, Akey JM, Foss E, Smith EN, Mackelprang R, Kruglyak L (2003) Trans-acting regulatory variation in Saccharomyces cerevisiae and the role of transcription factors. Nat Genet 35:57–64

    Article  PubMed  CAS  Google Scholar 

  85. Wayne ML, Mcintyre LM (2002) Combining mapping and arraying: an approach to candidate gene identification. Proc Natl Acad Sci U S A 99:14903–14906

    Article  PubMed  CAS  Google Scholar 

  86. Schadt EE, Monks SA, Drake TA, Lusis AJ, Che N, Colinayo V, Ruff TG, Milligan SB, Lamb JR, Cavet G, Linsley PS, Mao M, Stoughton RB, Friend SH (2003) Genetics of gene expression surveyed in maize, mouse and man. Nature 422:297–302

    Article  PubMed  CAS  Google Scholar 

  87. Twigger SN, Pasko D, Nie J, Shimoyama M, Bromberg S, Campbell D, Chen J, Dela Cruz N, Fan C, Foote C, Harris G, Hickmann B, Ji Y, Jin W, Li D, Mathis J, Nenasheva N, Nigam R, Petri V, Reilly D, Ruotti V, Schauberger E, Seiler K, Slyper R, Smith J, Wang W, Wu W, Zhao L, Zuniga-Meyer A, Tonellato PJ, Kwitek AE, Jacob HJ (2005) Tools and strategies for physiological genomics: the Rat Genome Database. Physiol Genomics 23:246–256

    Article  PubMed  CAS  Google Scholar 

  88. Bystrykh L, Weersing E, Dontje B, Sutton S, Pletcher MT, Wiltshire T, Su AI, Vellenga E, Wang J, Manly KF, Lu L, Chesler EJ, Alberts R, Jansen RC, Williams RW, Cooke MP, De Haan G (2005) Uncovering regulatory pathways that affect hematopoietic stem cell function using ‘genetical genomics’. Nat Genet 37:225–232

    Article  PubMed  CAS  Google Scholar 

  89. Chesler EJ, Lu L, Shou S, Qu Y, Gu J, Wang J, Hsu HC, Mountz JD, Baldwin NE, Langston MA, Threadgill DW, Manly KF, Williams RW (2005) Complex trait analysis of gene expression uncovers polygenic and pleiotropic networks that modulate nervous system function. Nat Genet 37:233–242

    Article  PubMed  CAS  Google Scholar 

  90. Hubner N, Wallace CA, Zimdahl H, Petretto E, Schulz H, Maciver F, Mueller M, Hummel O, Monti J, Zidek V, Musilova A, Kren V, Causton H, Game L, Born G, Schmidt S, Muller A, Cook SA, Kurtz TW, Whittaker J, Pravenec M, Aitman TJ (2005) Integrated transcriptional profiling and linkage analysis for identification of genes underlying disease. Nat Genet 37:243–253

    Article  PubMed  CAS  Google Scholar 

  91. Stassen AP, Groot PC, Eppig JT, Demant P (1996) Genetic composition of the recombinant congenic strains. Mamm Genome 7:55–58

    Article  PubMed  CAS  Google Scholar 

  92. Abiola O, Angel JM, Avner P, Bachmanov AA, Belknap JK, Bennett B, Blankenhorn EP, Blizard DA, Bolivar V, Brockmann GA, Buck KJ, Bureau JF, Casley WL, Chesler EJ, Cheverud JM, Churchill GA, Cook M, Crabbe JC, Crusio WE, Darvasi A, De Haan G, Dermant P, Doerge RW, Elliot RW, Farber CR, Flaherty L, Flint J, Gershenfeld H, Gibson JP, Gu J, Gu W, Himmelbauer H, Hitzemann R, Hsu HC, Hunter K, Iraqi FF, Jansen RC, Johnson TE, Jones BC, Kempermann G, Lammert F, Lu L, Manly KF, Matthews DB, Medrano JF, Mehrabian M, Mittlemann G, Mock BA, Mogil JS, Montagutelli X, Morahan G, Mountz JD, Nagase H, Nowakowski RS, O’hara BF, Osadchuk AV, Paigen B, Palmer AA, Peirce JL, Pomp D, Rosemann M, Rosen GD, Schalkwyk LC, Seltzer Z, Settle S, Shimomura K, Shou S, Sikela JM, Siracusa LD, Spearow JL, Teuscher C, Threadgill DW, Toth LA, Toye AA, Vadasz C, Van Zant G, Wakeland E, Williams RW, Zhang HG, Zou F (2003) The nature and identification of quantitative trait loci: a community’s view. Nat Rev Genet 4:911–916

    PubMed  Google Scholar 

  93. Westfall PH, Young SS (1993) Resampling based multiple testing: examples and methods for p-value adjustment. Wiley, New York

    Google Scholar 

  94. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodological 57:289–300

    Google Scholar 

  95. Datta S (2005) Empirical Bayes screening of many p-values with applications to microarray studies. Bioinformatics 21:1987–1994

    Article  PubMed  CAS  Google Scholar 

  96. Storey JD, Tibshirani R (2003) Statistical methods for identifying differentially expressed genes in DNA microarrays. Methods Mol Biol 224:149–157

    PubMed  CAS  Google Scholar 

  97. Reiner A, Yekutieli D, Benjamini Y (2003) Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics 19:368–375

    Article  PubMed  CAS  Google Scholar 

  98. Xie Y, Pan W, Khodursky AB (2005) A note on using permutation-based false discovery rate estimates to compare different analysis methods for microarray data. Bioinformatics 21:4280–4288

    Article  PubMed  CAS  Google Scholar 

  99. Gao X (2006) Construction of null statistics in permutation-based multiple testing for multi-factorial microarray experiments. Bioinformatics 22:1486–1494

    Article  PubMed  CAS  Google Scholar 

  100. Ploner A, Calza S, Gusnanto A, Pawitan Y (2006) Multidimensional local false discovery rate for microarray studies. Bioinformatics 22:556–565

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Research described in this article was supported by Philip Morris USA Inc. and Philip Morris International

Author information

Authors and Affiliations

  1. Laboratory of Neurobehavioral Genetics, Nathan S. Kline Institute for Psychiatric Research, 140 Old Orangeburg Road, Orangeburg, NY, 10962, USA

    Csaba Vadasz, Mariko Saito, Danielle O’Brien, Goutam Chakraborty & Ray Wang

  2. Department of Psychiatry, New York University School of Medicine, New York, NY, 10016, USA

    Csaba Vadasz & Mariko Saito

  3. Department of Pathology, New York University School of Medicine, New York, NY, 10016, USA

    Jiri Zavadil

  4. Genomics Facility, New York University Cancer Institute, New York, NY, 10016, USA

    Jiri Zavadil

  5. The Walter and Eliza Hall Institute of Medical Research, Parkville, Australia

    Grant Morahan

Authors
  1. Csaba Vadasz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mariko Saito
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Danielle O’Brien
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jiri Zavadil
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Grant Morahan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Goutam Chakraborty
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ray Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Csaba Vadasz.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vadasz, C., Saito, M., O’Brien, D. et al. Ventral Tegmental Transcriptome Response to Intermittent Nicotine Treatment and Withdrawal in BALB/cJ, C57BL/6ByJ, and Quasi-Congenic RQI Mice. Neurochem Res 32, 457–480 (2007). https://doi.org/10.1007/s11064-006-9250-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11064-006-9250-4

Keywords

Search

Navigation