GABA- and acetylcholine-related gene expression in blood correlate with tic severity and microarray evidence for alternative splicing in Tourette syndrome: A pilot study

Brain Research

Volumn 1381, Issue , 2011, Pages 228-236

  Tian, Yingfang ^a   Gunther, Joan R ^a   Liao, Isaac H ^a   Liu, Dazhi ^a   Ander, Bradley P ^a   Stamova, Boryana S ^a   Lit, Lisa ^a   Jickling, Glen C ^a   Xu, Huichun ^a   Zhan, Xinhua ^a   Sharp, Frank R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Acetylcholine; Alternative splicing; Blood; GABA; Gene expression profiling; Tourette syndrome

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; ACETYLCHOLINE; CARRIER PROTEIN; G PROTEIN COUPLED RECEPTOR; LEUKEMIA INHIBITORY FACTOR; NICOTINIC RECEPTOR; PHOSPHATE CYTIDYLYLTRANSFERASE 1; PHOSPHOLIPASE D1; PROTEIN SLC33A1; PROTEIN SLC5A7; PROTEIN SLC6A1; TRANSFERASE; UNCLASSIFIED DRUG;

ADOLESCENT; ALTERNATIVE RNA SPLICING; ARTICLE; BASAL GANGLION; CHILD; CHOLINERGIC NERVE CELL; CLINICAL ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DEMOGRAPHY; DISEASE SEVERITY; FEMALE; GENE EXPRESSION; GILLES DE LA TOURETTE SYNDROME; GLOBUS PALLIDUS; HUMAN; INTERNEURON; MALE; MICROARRAY ANALYSIS; PILOT STUDY; PRIORITY JOURNAL; SCHOOL CHILD; SEX DIFFERENCE; TIC;

ADOLESCENT; ALTERNATIVE SPLICING; ANALYSIS OF VARIANCE; CHILD; FEMALE; GENE EXPRESSION PROFILING; HUMANS; LEUKEMIA INHIBITORY FACTOR; MALE; PILOT PROJECTS; RECEPTORS, GABA-A; RECEPTORS, NICOTINIC; RNA; SEVERITY OF ILLNESS INDEX; TOURETTE SYNDROME;

EID: 79952280561     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2011.01.026     Document Type: Article

References (64)

1. A. Achiron, and M. Gurevich Peripheral blood gene expression signature mirrors central nervous system disease: the model of multiple sclerosis Autoimmun. Rev. 5 2006 517 522 (Pubitemid 44486947)
2. R.L. Albin, and J.W. Mink Recent advances in Tourette syndrome research Trends Neurosci. 29 2006 175 182
3. APA, 2000. Diagnostic and Statistical Manual of Mental Disorders, 4th edn. text revision. American Psychiatric Association, Washington, DC.
4. S. Bauer Cytokine control of adult neural stem cells Ann. NY Acad. Sci. 1153 2009 48 56
5. C.L. Baym, B.A. Corbett, S.B. Wright, and S.A. Bunge Neural correlates of tic severity and cognitive control in children with Tourette syndrome Brain 131 2008 165 179
6. Bhat, R., Axtell, R., Mitra, A., Miranda, M., Lock, C., Tsien, R.W., Steinman, L., 2010. Inhibitory role for GABA in autoimmune inflammation. Proc. Natl Acad. Sci. USA 107, 2580-2585.
7. H. Bjurstom, J. Wang, I. Ericsson, M. Bengtsson, Y. Liu, S. Kumar-Mendu, S. Issazadeh-Navikas, and B. Birnir GABA, a natural immunomodulator of T lymphocytes J. Neuroimmunol. 205 2008 44 50
8. D.L. Black Mechanisms of alternative pre-messenger RNA splicing Annu. Rev. Biochem. 72 2003 291 336 (Pubitemid 36930448)
9. M.H. Bloch, J.F. Leckman, H. Zhu, and B.S. Peterson Caudate volumes in childhood predict symptom severity in adults with Tourette syndrome Neurology 65 2005 1253 1258 (Pubitemid 41508219)
10. A.R. Calver, D. Michalovich, T.T. Testa, M.J. Robbins, C. Jaillard, J. Hill, P.G. Szekeres, K.J. Charles, S. Jourdain, J.D. Holbrook, I. Boyfield, N. Patel, A.D. Medhurst, and M.N. Pangalos Molecular cloning and characterisation of a novel GABAB-related G-protein coupled receptor Brain Res. Mol. Brain Res. 110 2003 305 317 (Pubitemid 36184703)
11. K.J. Charles, A.R. Calver, S. Jourdain, and M.N. Pangalos Distribution of a GABAB-like receptor protein in the rat central nervous system Brain Res. 989 2003 135 146 (Pubitemid 37211418)
12. S.S. Cheema, L. Richards, M. Murphy, and P.F. Bartlett Leukemia inhibitory factor prevents the death of axotomised sensory neurons in the dorsal root ganglia of the neonatal rat J. Neurosci. Res. 37 1994 213 218 (Pubitemid 24054649)
13. S.S. Cheema, L.J. Richards, M. Murphy, and P.F. Bartlett Leukaemia inhibitory factor rescues motoneurones from axotomy-induced cell death NeuroReport 5 1994 989 992 (Pubitemid 24138116)
14. Z.W. Chen, and R.W. Olsen GABAA receptor associated proteins: a key factor regulating GABAA receptor function J. Neurochem. 100 2007 279 294 (Pubitemid 46010990)
15. J.A. Clark, E. Mezey, A.S. Lam, and T.I. Bonner Distribution of the GABA(B) receptor subunit gb2 in rat CNS Brain Res. 860 2000 41 52 (Pubitemid 30155836)
16. J.A. Dani Overview of nicotinic receptors and their roles in the central nervous system Biol. Psychiatry 49 2001 166 174 (Pubitemid 32178425)
17. Dionisio, L., Josede Rosa, M., Bouzat, C., Esandi, M.D., 2011. An intrinsic GABAergic system in human lymphocytes. Neuropharmacology. 60, 513-519.
18. J.M. Fritschy, C. Sidler, F. Parpan, M. Gassmann, K. Kaupmann, B. Bettler, and D. Benke Independent maturation of the GABA(B) receptor subunits GABA(B1) and GABA(B2) during postnatal development in rodent brain J. Comp. Neurol. 477 2004 235 252 (Pubitemid 39129610)
19. S.J. Glatt, I.P. Everall, W.S. Kremen, J. Corbeil, R. Sasik, N. Khanlou, M. Han, C.C. Liew, and M.T. Tsuang Comparative gene expression analysis of blood and brain provides concurrent validation of SELENBP1 up-regulation in schizophrenia Proc. Natl Acad. Sci. USA 102 2005 15533 15538 (Pubitemid 41528092)
20. R. Hirunsatit, E.D. George, B.K. Lipska, H.M. Elwafi, L. Sander, C.M. Yrigollen, J. Gelernter, E.L. Grigorenko, J. Lappalainen, S. Mane, A.C. Nairn, J.E. Kleinman, and A.A. Simen Twenty-one-base-pair insertion polymorphism creates an enhancer element and potentiates SLC6A1 GABA transporter promoter activity Pharmacogenet. Genomics 19 2009 53 65
21. J.J. Hong, C.R. Loiselle, D.Y. Yoon, O. Lee, K.G. Becker, and H.S. Singer Microarray analysis in Tourette syndrome postmortem putamen J. Neurol. Sci. 225 2004 57 64 (Pubitemid 39311710)
22. T.C. Jacob, S.J. Moss, and R. Jurd GABA(A) receptor trafficking and its role in the dynamic modulation of neuronal inhibition Nat. Rev. Neurosci. 9 2008 331 343 (Pubitemid 351556042)
23. J. Jimenez-Shahed Tourette syndrome Neurol. Clin. 27 2009 737 755 (vi)
24. I.W. Jones, J.P. Bolam, and S. Wonnacott Presynaptic localisation of the nicotinic acetylcholine receptor beta2 subunit immunoreactivity in rat nigrostriatal dopaminergic neurones J. Comp. Neurol. 439 2001 235 247 (Pubitemid 32906025)
25. P.S. Kalanithi, W. Zheng, Y. Kataoka, M. DiFiglia, H. Grantz, C.B. Saper, M.L. Schwartz, J.F. Leckman, and F.M. Vaccarino Altered parvalbumin-positive neuron distribution in basal ganglia of individuals with Tourette syndrome Proc. Natl Acad. Sci. USA 102 2005 13307 13312 (Pubitemid 41325019)
26. Kataoka, Y., Kalanithi, P.S., Grantz, H., Schwartz, M.L., Saper, C., Leckman, J.F., Vaccarino, F.M., 2010. Decreased number of parvalbumin and cholinergic interneurons in the striatum of individuals with Tourette syndrome. J. Comp. Neurol. 518, 277-291.
27. K. Kawashima, and T. Fujii The lymphocytic cholinergic system and its contribution to the regulation of immune activity Life Sci. 74 2003 675 696 (Pubitemid 37494897)
28. K. Kawashima, and T. Fujii The lymphocytic cholinergic system and its biological function Life Sci. 72 2003 2101 2109 (Pubitemid 36298953)
29. R. Kimura, N. Ushiyama, T. Fujii, and K. Kawashima Nicotine-induced Ca2+ signaling and down-regulation of nicotinic acetylcholine receptor subunit expression in the CEM human leukemic T-cell line Life Sci. 72 2003 2155 2158 (Pubitemid 36298962)
30. J.F. Leckman, M.A. Riddle, M.T. Hardin, S.I. Ort, K.L. Swartz, J. Stevenson, and D.J. Cohen The Yale Global Tic Severity Scale: initial testing of a clinician-rated scale of tic severity J. Am. Acad. Child Adolesc. Psychiatry 28 1989 566 573 (Pubitemid 19196295)
31. J.F. Leckman, M.H. Bloch, L. Scahill, and R.A. King Tourette syndrome: the self under siege J. Child Neurol. 21 2006 642 649 (Pubitemid 44295122)
32. J.F. Leckman, F.M. Vaccarino, P.S. Kalanithi, and A. Rothenberger Annotation: Tourette syndrome: a relentless drumbeat - driven by misguided brain oscillations J. Child Psychol. Psychiatry 47 2006 537 550 (Pubitemid 43744784)
33. R. Lemke, R.A. Gadient, P.H. Patterson, V. Bigl, and R. Schliebs Leukemia inhibitory factor (LIF) mRNA-expressing neuronal subpopulations in adult rat basal forebrain Neurosci. Lett. 229 1997 69 71 (Pubitemid 27306859)
34. Liao, I.H., Sharp, F.R., 2010. Tourette syndrome: gene expression as a tool to discover drug targets. Neurotherapeutics 7, 302-306.
35. L. Lit, D.L. Gilbert, W. Walker, and F.R. Sharp A subgroup of Tourette's patients overexpress specific natural killer cell genes in blood: a preliminary report Am. J. Med. Genet. B Neuropsychiatr. Genet. 144B 2007 958 963 (Pubitemid 47548000)
36. L. Lit, A. Enstrom, F.R. Sharp, and D.L. Gilbert Age-related gene expression in Tourette syndrome J. Psychiatr. Res. 43 2009 319 330
37. F.H. Marshall The role of GABA(B) receptors in the regulation of excitatory neurotransmission Results Probl. Cell Differ. 44 2008 87 98
38. D. Martino, R.C. Dale, D.L. Gilbert, G. Giovannoni, and J.F. Leckman Immunopathogenic mechanisms in Tourette syndrome: a critical review Mov. Disord. 24 2009 1267 1279
39. D.S. McGehee, and L.W. Role Physiological diversity of nicotinic acetylcholine receptors expressed by vertebrate neurons Annu. Rev. Physiol. 57 1995 521 546
40. M. Michikawa, S. Kikuchi, and S.U. Kim Leukemia inhibitory factor (LIF) mediated increase of choline acetyltransferase activity in mouse spinal cord neurons in culture Neurosci. Lett. 140 1992 75 77
41. J. Mohrluder, M. Schwarten, and D. Willbold Structure and potential function of gamma-aminobutyrate type A receptor-associated protein FEBS J. 276 2009 4989 5005
42. N. Muller Tourette's syndrome: clinical features, pathophysiology, and therapeutic approaches Dialogues Clin. Neurosci. 9 2007 161 171 (Pubitemid 47075464)
43. Paquette, J., Tokuyasu, T., 2010. EGAN: exploratory gene association networks. Bioinformatics 26, 285-286.
44. B.S. Peterson, P. Thomas, M.J. Kane, L. Scahill, H. Zhang, R. Bronen, R.A. King, J.F. Leckman, and L. Staib Basal ganglia volumes in patients with Gilles de la Tourette syndrome Arch. Gen. Psychiatry 60 2003 415 424 (Pubitemid 36403003)
45. W.D. Phillips, and S.C. Froehner GABARAP and GABA(A) receptor clustering Neuron 33 2002 4 6
46. M.J. Rane, D. Gozal, W. Butt, E. Gozal, W.M. Pierce Jr., S.Z. Guo, R. Wu, A.D. Goldbart, V. Thongboonkerd, K.R. McLeish, and J.B. Klein Gamma-amino butyric acid type B receptors stimulate neutrophil chemotaxis during ischemia-reperfusion J. Immunol. 174 2005 7242 7249 (Pubitemid 40705693)
47. M.D. Robinson, and T.P. Speed A comparison of Affymetrix gene expression arrays BMC Bioinform. 8 2007 449
48. L.W. Role, and D.K. Berg Nicotinic receptors in the development and modulation of CNS synapses Neuron 16 1996 1077 1085 (Pubitemid 26227229)
49. J.S. Rudge, M.J. Eaton, P. Mather, R.M. Lindsay, and S.R. Whittemore CNTF induces raphe neuronal precursors to switch from a serotonergic to a cholinergic phenotype in vitro Mol. Cell. Neurosci. 7 1996 204 221 (Pubitemid 26171284)
50. F.R. Sharp, L. Lit, H. Xu, M. Apperson, W. Walker, B. Wong, D.L. Gilbert, A. Hershey, and T.A. Glauser Genomics of brain and blood: progress and pitfalls Epilepsia 47 2006 1603 1607 (Pubitemid 44556392)
51. F.R. Sharp, H. Xu, L. Lit, W. Walker, M. Apperson, D.L. Gilbert, T.A. Glauser, B. Wong, A. Hershey, D.Z. Liu, J. Pinter, X. Zhan, X. Liu, and R. Ran The future of genomic profiling of neurological diseases using blood Arch. Neurol. 63 2006 1529 1536 (Pubitemid 44748794)
52. H.S. Singer Tourette's syndrome: from behaviour to biology Lancet Neurol. 4 2005 149 159 (Pubitemid 40269145)
53. S.P. Singh, R. Kalra, P. Puttfarcken, A. Kozak, J. Tesfaigzi, and M.L. Sopori Acute and chronic nicotine exposures modulate the immune system through different pathways Toxicol. Appl. Pharmacol. 164 2000 65 72 (Pubitemid 30198545)
54. Soilu-Hanninen, M., Broberg, E., Roytta, M., Mattila, P., Rinne, J., Hukkanen, V., 2010. Expression of LIF and LIF receptor beta in Alzheimer's and Parkinson's diseases. Acta Neurol. Scand. 121, 44-50.
55. A.A. Stillman, Z. Krsnik, J. Sun, M.R. Rasin, M.W. State, N. Sestan, and A. Louvi Developmentally regulated and evolutionarily conserved expression of SLITRK1 in brain circuits implicated in Tourette syndrome J. Comp. Neurol. 513 2009 21 37
56. P.F. Sullivan, C. Fan, and C.M. Perou Evaluating the comparability of gene expression in blood and brain Am. J. Med. Genet. B Neuropsychiatr. Genet. 141B 2006 261 268
57. J.E. Swain, L. Scahill, P.J. Lombroso, R.A. King, and J.F. Leckman Tourette syndrome and tic disorders: a decade of progress J. Am. Acad. Child Adolesc. Psychiatry 46 2007 947 968 (Pubitemid 47220680)
58. Y. Tang, D.L. Gilbert, T.A. Glauser, A.D. Hershey, and F.R. Sharp Blood gene expression profiling of neurologic diseases: a pilot microarray study Arch. Neurol. 62 2005 210 215 (Pubitemid 40204742)
59. J. Tian, Y. Lu, H. Zhang, C.H. Chau, H.N. Dang, and D.L. Kaufman Gamma-aminobutyric acid inhibits T cell autoimmunity and the development of inflammatory responses in a mouse type 1 diabetes model J. Immunol. 173 2004 5298 5304 (Pubitemid 39387814)
60. Y. Tian, P.G. Green, B. Stamova, I. Hertz-Picciotto, I.N. Pessah, R. Hansen, X. Yang, J.P. Gregg, P. Ashwood, G. Jickling, J. Van de Water, and F.R. Sharp Correlations of gene expression with blood lead levels in children with autism compared to typically developing controls Neurotox. Res. 19 2011 1 13
61. J.T. Walkup, M.C. LaBuda, H.S. Singer, J. Brown, M.A. Riddle, and O. Hurko Family study and segregation analysis of Tourette syndrome: evidence for a mixed model of inheritance Am. J. Hum. Genet. 59 1996 684 693 (Pubitemid 26269047)
62. S. Wonnacott Presynaptic nicotinic ACh receptors Trends Neurosci. 20 1997 92 98 (Pubitemid 27050704)
63. A. Zhang Advanced Analysis of Gene Expression Microarray Data 2006 World Scientific Press Singapore; Hackensack, N.J.
64. F.M. Zhou, C.J. Wilson, and J.A. Dani Cholinergic interneuron characteristics and nicotinic properties in the striatum J. Neurobiol. 53 2002 590 605 (Pubitemid 35375589)