Allelic Variation of Calsyntenin 2 (CLSTN2) Modulates the Impact of Developmental Tobacco Smoke Exposure on Mnemonic Processing in Adolescents

Biological Psychiatry

Volumn 65, Issue 8, 2009, Pages 671-679

  Jacobsen, Leslie K ^a,b,c   Picciotto, Marina R ^a   Heath, Christopher J ^a   Mencl, W Einar ^c   Gelernter, Joel ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HASKINS LABORATORIES   (United States)

Author keywords

Adolescent; calsyntenin 2; nicotine; parahippocampal gyrus; prenatal; verbal memory

Indexed keywords

TOBACCO SMOKE;

ADOLESCENT; ALLELE; ARTICLE; BRAIN DEVELOPMENT; BRAIN FUNCTION; BRAIN REGION; CLINICAL ARTICLE; CLSTN2 GENE; CONTROLLED STUDY; FEMALE; GENE; GENE INTERACTION; GENETIC VARIABILITY; HUMAN; KIBRA GENE; MALE; PRENATAL EXPOSURE; PRIORITY JOURNAL; TEMPORAL LOBE; VERBAL MEMORY; VISUAL MEMORY;

ADOLESCENT; ADOLESCENT BEHAVIOR; ADOLESCENT DEVELOPMENT; ALLELIC IMBALANCE; BRAIN; CALCIUM-BINDING PROTEINS; FEMALE; GENOTYPE; HUMANS; MALE; MEMBRANE PROTEINS; MEMORY DISORDERS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROTEINS; TEMPORAL LOBE; TOBACCO SMOKE POLLUTION;

EID: 62749154932     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2008.10.024     Document Type: Article

References (63)

1. Slotkin T.A. Cholinergic systems in brain development and disruption by neurotoxicants: Nicotine, environmental tobacco smoke, organophosphates. Toxico Appl Pharmacol 198 (2004) 132-151
2. Liang K., Poytress B.S., Chen Y., Leslie F.M., Weinberger N.M., and Metherate R. Neonatal nicotine exposure impairs nicotine enhancement of central auditory processing and auditory learning in adult rats. Eur J Neurosci 24 (2006) 857-866
3. King S.L., Marks M.J., Grady S.R., Caldarone B.J., Koren A.O., Mukhin A.G., et al. Conditional expression in corticothalamic efferents reveals a developmental role for nicotininc acetylcholine receptors in modulation of passive avoidance behavior. J Neurosci 23 (2003) 3837-3843
4. Navarro H.A., Seidler F.J., Eylers J.P., Baker F.E., Dobbins S.S., Lappi S.E., et al. Effects of prenatal nicotine exposure on development of central and peripheral cholinergic neurotransmitter systems. Evidence for cholinergic trophic influences in developing brain. J Pharmacol Exp Ther 251 (1989) 894-900
5. Slotkin T.A., MacKillop E.A., Rudder C.L., Ryde I.T., Tate C.A., and Seidler F.J. Permanent, sex-selective effects of prenatal or adolescent nicotine exposure, separately or sequentially, in rat brain regions: Indices of cholinergic and serotonergic synaptic function, cell signaling, and neural cell number and size at 6 months of age. Neuropsychopharmacology 32 (2007) 1082-1097
6. Jacobsen L.K., Slotkin T.A., Mencl W.E., Frost S.J., and Pugh K.R. Gender-specific effects of prenatal and adolescent exposure to tobacco smoke on auditory and visual attention. Neuropsychopharmacology 32 (2007) 2453-2464
7. McCartney J.S., Fried P.A., and Watkinson B. Central auditory processing in school-age children prenatally exposed to cigarette smoke. Neurotoxicol Teratol 16 (1994) 269-276
8. Jacobsen L.K., Mencl W.E., Constable R.T., Westerveld M., and Pugh K.R. Impact of smoking abstinence on working memory neurocircuitry in adolescent daily tobacco smokers. Psychopharmacology (Berl) 193 (2007) 557-566
9. Jacobsen L.K., Krystal J.H., Mencl W.E., Westerveld M., Frost S.J., and Pugh K.R. Effects of smoking and smoking abstinence on cognition in adolescent tobacco smokers. Biol Psychiatry 57 (2005) 56-66
10. Jacobsen L.K., Slotkin T.A., Westerveld M., Mencl W.E., and Pugh K.R. Visuospatial memory deficits emerging during nicotine withdrawal in adolescents with prenatal exposure to active maternal smoking. Neuropsychopharmacology 31 (2006) 1550-1561
11. Jacobsen L.K., Pugh K.R., Mencl W.E., and Gelernter J. C957T polymophism of the dopamine D2 receptor gene modulates the effect of nicotine on working memory performance and cortical processing efficiency. Psychopharmacology (Berl) 188 (2006) 530-540
12. Squire L.R. Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans. Psychol Rev 99 (1992) 195-231
13. Eichenbaum H., Schoenbaum G., Young B., and Bunsey M. Functional organization of the hippocampal memory system. Proc Natl Acad Sci U S A 93 (1996) 13500-13507
14. Papassotiropoulos A., Stephan D.A., Huentelman M.J., Hoerndli F.J., Craig D.W., Pearson J.V., et al. Common KIBRA alleles are associated with human memory performance. Science 314 (2006) 475-478
15. Schaper K., Kolsch H., Popp J., Wagner M., and Jessen F. KIBRA gene variants are associated with episodic memory in healthy elderly. Neurobiol Aging 29 (2008) 1123-1125
16. Almeida O.P., Schwab S.G., Lautenschlager N.T., Morar B., Greenop K.R., Flicker L., and Wildenauer D. KIBRA genetic polymorphism influences episodic memory in later life, but does not increase the risk of mild cognitive impairment. J Cell Mol Med 12 (2008) 1672-1676
17. Wagner K., Frings L., Halsband U., Everts R., Buller A., Spreer J., et al. Hippocampal functional connectivity reflects verbal episodic memory network integrity. Neuroreport 18 (2007) 1719-1723
18. Sederberg P.B., Schulze-Bonhage A., Madsen J.R., Bromfield E.B., McCarthy D.C., Brandt A., et al. Hippocampal and neocortical gamma oscillations predict memory formation in humans. Cereb Cortex 17 (2007) 1190-1196
19. Karlsgodt K.H., Shirinyan D., van Erp T.G.M., Cohen M.S., and Cannon T.D. Hippocampal activations during encoding and retrieval in a verbal working memory paradigm. Neuroimage 25 (2005) 1224-1231
20. Bunge S.A., Burrows B., and Wagner A.D. Prefrontal and hippocampal contributions to visual associative recognition: Interactions between cognitive control and episodic retrieval. Brain Cogn 56 (2004) 141-152
21. Kremerskothen J., Plaas C., Buther K., Finger I., Veltel S., Matanis T., et al. Characterization of KIBRA, a novel WW domain-containing protein. Biochem Biophys Res Comm 300 (2003) 862-867
22. Hintsch G., Zurlinden A., Meskenaite V., Steuble M., Fink-Widmer K., Kinter J., et al. The calsyntenins-a family of postsynaptic membrane proteins with distinct neuronal expression patterns. Mol Cell Neurosci 21 (2002) 393-409
23. Ikeda D.D., Duan Y., Matsuki M., Kunitomo H., Hutter H., Hedgecock E.M., et al. CASY-1, an ortholog of calsyntenins/alcadeins, is essential for learning in Caenorhabditis elegans. Proc Natl Acad Sci U S A 105 (2008) 5260-5265
24. Araki Y., Tomita S., Yamaguchi H., Miyagi N., Sumioka A., Kirino Y., et al. Novel cadherin-related membrane proteins, alcadeins, enhance the XII-like protein-mediated stabilization of amyloid β-protein precursor metabolism. J Biol Chem 278 (2003) 49448-49458
25. Araki Y., Kawano T., Taru H., Saito Y., Wada S., Miyamoto K., et al. The novel cargo alcadein induces vesicle association of kinesin-1 motor components and activates axonal transport. EMBO J 26 (2007) 1475-1486
26. Snyder E.M., Nong Y., Almeida C.G., Paul S., Moran T., Choi E.Y., et al. Regulation of NMDA receptor trafficking by amyloid-β. Nat Neurosci 8 (2005) 1051-1058
27. Nie H., Li Z., Lukas R.J., Shen Y., Song L., Wang X., et al. Construction of SH-EP1-α4β2-hAPP695 cell line and effects of nicotinic agonstis on β-amyloid in the cells. Cell Mol Neurobiol 28 (2008) 103-112
28. Kaufman J., Birmaher B., Brent D., Rao U., Flynn C., Moreci P., et al. Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): Initial reliability and validity data. J Am Acad Child Adolesc Psychiatry 36 (1997) 980-988
29. Meyers K., McLellan A.T., Jaeger J.L., and Pettinati H.M. The development of the comprehensive addiction severity index for adolescents (CASI-A). An interview for assessing multiple problems of adolescents. J Subst Abuse Treat 12 (1995) 181-193
30. Jacobsen L.K., Picciotto M.R., Heath C.J., Frost S.J., Tsou K.A., Dwan R.A., et al. Prenatal and adolescent exposure to tobacco smoke modulates the development of white matter microstructure. J Neurosci 27 (2007) 13491-13498
31. Shiffman S., Paty J.A., Gnys M., Kassel J.D., and Elash C. Nicotine withdrawal in chippers and regular smokers: Subjective and cognitive effects. Health Psychol 14 (1995) 301-309
32. Shapiro A.M., Benedict R.H., Schretlen D., and Brandt J. Construct and concurrent validity of the Hopkins Verbal Learning Test-revised. Clin Neuropsychol 13 (1999) 348-358
33. Loring D.W., and Meador K.J. The Medical College of Georgia (MCG) Complex Figures: Four forms for follow-up. In: Knight J.A. (Ed). The Handbook of Rey-Osterreith Complex Figure Usage: Clinical and Research Application (2003), Psychological Assessment Resources, Lutz, FL
34. Shi M.M., Myrand S.P., Bleavins M.R., and de la Iglesia F.A. High throughput genotyping for the detection of a single nucleotide polymorphism in NAD(P)H quinone oxidoreductase (DT diaphorase) using TaqMan probes. Mol Pathol 52 (1999) 295-299
35. Friston K.J., Ashburner J., Frith C.D., Poline J.B., Heather J.D., and Frackowiak R.S. Spatial registration and normalization of images. Hum Brain Mapp 2 (1995) 165-189
36. Visscher K.M., Miezin F.M., Kelly J.E., Buckner R.L., Donaldson D.I., McAvoy M.P., et al. Mixed blocked/event-related designs separate transient and sustained activity in fMRI. Neuroimage 19 (2003) 1694-1708
37. Boynton G.M., Engel S.A., Glover G.H., and Heeger D.J. Linear systems analysis of functional magnetic resonance imaging in human VI. J Neurosci 16 (1996) 4207-4221
38. Genovese C.R., Lazar N.A., and Nichols T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15 (2002) 870-878
39. Friston K.J. Functional and effective connectivity in neuroimaging: A synthesis. Hum Brain Mapp 2 (1994) 56-57
40. McIntosh A.R., Bookstein F.L., Haxby J.V., and Grady C.L. Spatial pattern analysis of functional brain images using partial least squares. Neuroimage 3 (1996) 143-157
41. Heatherton T.F., Kozlowski L.T., Frecker R.C., and Fagerstrom K.O. The Fagerstrom Test for Nicotine Dependence: A revision of the Fagerstrom Tolerance Questionnaire. Br J Addic 86 (1991) 1119-1127
42. Araki Y., Miyagi N., Kato N., Yoshida T., Wada S., Nishimura M., et al. Coordinated metabolism of alcadein and amyloid β-protein precursor regulates FE65-dependent gene transactivation. J Biol Chem 279 (2004) 24343-24354
43. Selkoe D.J. Folding proteins in fatal ways. Nature 426 (2003) 900-904
44. Naslund J., Haroutunian V., Mohs R., Davis K.L., Davies P., Greengard P., et al. Correlation between elevated levels of amyloid beta-peptide in the brain and cognitive decline. JAMA 283 (2000) 1571-1577
45. Ma Q.H., Futagawa T., Yang W.L., Jiang X.D., Zeng L., Takeda Y., et al. The TAG1-APP signalling pathway through Fe65 negatively modulates neurogenesis. Nat Cell Biol 10 (2008) 283-294
46. Kim S.H., Kim Y.K., Jeong S.J., Haass C., Kim Y.H., and Suh Y.H. Enhanced release of secreted form of Alzheimer's amyloid precursor protein from PC12 cells by nicotine. Mol Pharmacol 52 (1997) 430-436
47. Efthimiopoulos S., Vassiacopouou D., Ripellino J.A., Tezapsidis N., and Robakis N.K. Cholinergic agonists stimulate secretion of soluble full-length amyloid precursor protein in neuroendocrine cells. Proc Natl Acad Sci U S A 93 (1996) 8046-8050
48. Utsuki T., Shoaib M., Holloway H.W., Ingram D.K., Wallace W.C., Haroutunian V., et al. Nicotine lowers the secretion of Alzheimer's amyloid beta-protein precursor that contains amyloid beta-peptide in rat. J Alzheimers Dis 4 (2002) 405-415
49. Oddo S., and LaFerla F.M. The role of nicotinic acetylcholine receptors in Alzheimer's disease. J Physiol 99 (2006) 172-179
50. Gonsalves B.D., Kahn I., Curran T., Norman D.A., and Wagner A.D. Memory strength and repetition suppression: Multimodal imaging of medial temporal cortical contributions to recognition. Neuron 47 (2005) 751-761
51. Brown M.W., and Xiang J.Z. Recognition memory: Neuronal substrates of the judgement of prior occurrence. Prog Neurobiol 55 (1998) 149-189
52. Weis S., Specht K., Klaver P., Tendolkar I., Willmes K., Ruhlmann J., et al. Process dissociation between contextual retrieval and item recognition. Neuroreport 15 (2004) 2729-2733
53. Henson R.N.A., Hornberger M., and Rugg M.D. Further dissociating the processes involved in recognition memory: An fMRI study. J Cogn Neurosci 17 (2005) 1058-1073
54. Buckner R.L., and Wheeler M.E. The cognitive neuroscience of remembering. Nat Rev Neurosci 2 (2001) 624-634
55. McDermott K.B., Jones T.C., Petersoen S.E., Lageman S.K., and Roediger H.L. Retrieval success is accompanied by enhanced activation in anterior prefrontal cortex during recognition memory: An event-related fMRI study. J Cogn Neurosci 12 (2000) 965-976
56. Henson R.N., Rugg M.D., Shallice T., and Dolan R.J. Confidence in recognition memory for words: Dissociating right prefrontal roles in episodic retrieval. J Cogn Neurosci 12 (2000) 913-923
57. Kuhl B.A., Dudukovic N.M., Kahn I., and Wagner A.D. Decreased demands on cognitive control reveal the neural processing benefits of forgetting. Nat Neurosci 10 (2007) 908-914
58. Eichenbaum H. A cortical-hippocampal system for declarative memory. Nat Rev Neurosci 1 (2000) 41-50
59. Eichenbaum H. Remembering: Functional organization of the declarative memory system. Curr Biol 16 (2006) R643-R645
60. Squire L.R., and Zola S.M. Episodic memory, semantic memory, and amnesia. Hippocampus 8 (1998) 205-211
61. Buka S.L., Goldstein J.M., Spartos E., and Tsuang M.T. The retrospective measurement of prenatal and perinatal events: Accuracy of maternal recall. Schizophr Res 71 (2004) 417-426
62. Beck A.T., Ward C.H., Mendelson M., Mock J., and Erbaugh J. An inventory for measuring depression. Arch Gen Psychiatry 4 (1961) 561-571
63. Conners C.K. Rating scales in attention-deficit/hyperactivity disorder: use in assessment and treatment monitoring. J Clin Psychiatry 59 suppl 7 (1998) 24-30