Strain and regional dependence of alternate splicing of acetylcholinesterase in the murine brain following stress or treatment with diisopropylfluorophosphate

Behavioural Brain Research

Volumn 210, Issue 1, 2010, Pages 107-115

  Livneh, Uri ^a   Dori, Amir ^b   Katzav, Aviva ^b   Kofman, Ora ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b SHEBA MEDICAL CENTER   (Israel)

Author keywords

Acetylcholinesterase; Alternative splicing; Anxiety; Butyrylcholinesterase; Depression; Elevated plus maze; Forced swim; Mouse strains; Paraoxonase

Indexed keywords

ACETYLCHOLINESTERASE; DYFLOS;

ALTERNATIVE RNA SPLICING; AMYGDALOID NUCLEUS; ANXIETY; ARTICLE; BAGG ALBINO MOUSE; C57BL 6 MOUSE; CONTROLLED STUDY; CORPUS STRIATUM; DEPRESSION; ENZYME ACTIVITY; EXPLORATORY BEHAVIOR; FORCED SWIMMING TEST; FRONTAL CORTEX; GENE EXPRESSION; HIPPOCAMPUS; LOCOMOTION; MAZE TEST; MOUSE; NONHUMAN; PRIORITY JOURNAL; STRAIN DIFFERENCE;

ACETYLCHOLINESTERASE; ALTERNATIVE SPLICING; ANIMALS; BRAIN; CHOLINESTERASE INHIBITORS; EXPLORATORY BEHAVIOR; FEMALE; ISOFLUROPHATE; MALE; MAZE LEARNING; MICE; MICE, INBRED BALB C; MICE, INBRED C3H; MICE, INBRED C57BL; MOTOR ACTIVITY; PROTEIN ISOFORMS; RANDOM ALLOCATION; RNA, MESSENGER; SPECIES SPECIFICITY; STRESS, PSYCHOLOGICAL;

EID: 77949567203     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2010.02.029     Document Type: Article

References (68)

1. Acquas E., Wilson C., Fibiger H.C. Conditioned and unconditioned stimuli increase frontal cortical and hippocampal acetylcholine release: effects of novelty, habituation and fear. J Neurosci 1996, 16:3089-3096.
2. Adamec R., Head D., Soreq H., Blundell J. The role of the read through variant of acetylcholinesterase in anxiogenic effects of predator stress in mice. Behav Brain Res 2008, 189:180-190.
3. Amat J., Baratta M.V., Paul E., Bland S.T., Watkins L.R., Maier S.F. Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nat Neurosci 2005, 8:365-371.
4. Amat J., Paul E., Watkins L.R., Maier S.F. Activation of the ventral medial prefrontal cortex during an uncontrollable stressor reproduces both the immediate and long-term protective effects of behavioral control. Neuroscience 2008, 154:1178-1186.
5. Amat J., Paul E., Zarza C., Watkins L.R., Maier S.F. Previous experience with behavioral control over stress blocks the behavioral and dorsal raphe nucleus activating effects of later uncontrollable stress: role of the ventral medial prefrontal cortex. J Neurosci 2006, 26:13264-13272.
6. Anisman H., Hayley S., Kelly O., Borowski T., Merali Z. Psychogenic, neurogenic, and systemic stressor effects on plasma corticosterone and behavior: mouse strain-dependent outcomes. Behav Neurosci 2001, 115:443-454.
7. Bertoglio L.J., Anzini C., Lino-de-Oliveira C., Carobrez A.P. Enhanced dorsolateral periaqueductal gray activity counteracts the anxiolytic response to midazolam on the elevated plus-maze Trial 2 in rats. Behav Brain Res 2005, 162:99-107.
8. Berton O., McClung C.A., Dileone R.J., Krishnan V., Renthal W., Russo S.J., et al. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 2006, 311:864-868.
9. Birikh K.R., Sklan E.H., Shoham S., Soreq H. Interaction of " readthrough" acetylcholinesterase with RACK1 and PKC II correlates with intensified fear-induced conflict behavior. Proc Natl Acad Sci USA 2003, 100:283-288.
10. Brooks S.P., Pask T., Jones L., Dunnett S.B. Behavioural profiles of inbred mouse strains used as transgenic backgrounds. II: cognitive tests. Genes Brain and Behav 2005, 4:307-317.
11. Browne R.O., Moyal-Segal L.B., Zumsteg D., David Y., Kofman O., Berger A., et al. Coding region paraoxonase polymorphisms dictate accentuated neuronal reactions in chronic, sub-threshold pesticide exposure. FASEB J 2006, 20:1733-1735.
12. Bustin S.A. Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J Mol Endocrinol 2000, 25:169-193.
13. Caldji C., Diorio J., Anisman H., Meaney M.J. Maternal behavior regulates benzodiazepine/GABAA receptor subunit expression in brain regions associated with fear in BALB/c and C57BL/6 mice. Neuropsychopharmacology 2004, 29:1344-1352.
14. Carobrez A.P., Bertoglio L.J. Ethological and temporal analyses of anxiety-like behavior: the elevated plus-maze model 20 years on. Neurosci Biobehav Rev 2005, 29:1193-1205.
15. Ceccarrelli I., Casamenti F., Massafra C., Pepeu G., Scali C., Aloisi A.M. Effects of novelty and pain on behavior and hippocampal ACh levels in male and female rats. Brain Res 1999, 815:169-176.
16. Cervo L., Canetta A., Calcagno E., Burbassi S., Sacchetti G., Caccia S., et al. Genotype-dependent activity of tryptophan hydroxylase-2 determines the response to citalopram in a mouse model of depression. J Neurosci 2005, 25:8165-8172.
17. Chapillon P., Manneche C., Belzung C., Caston J. Rearing environmental enrichment in two inbred strains of mice: 1. Effects on emotional reactivity. Behav Genet 1999, 29:41-46.
18. Chau D.T., Rada P., Kosloff R.A., Taylor J.L., Hoebel B.G. Nucleus accumbens muscarinic receptors in the control of behavioral depression: antidepressant-like effects of local M1 antagonist in the Porsolt swim test. Neuroscience 2001, 104:791-798.
19. Cohen O., Reichenberg A., Perry C., Ginzberg D., Pollmacher T., Soreq H., et al. Endotoxin-induced changes in human working and declarative memory associate with cleavage of plasma " readthrough" acetylcholinesterase. J Mol Neurosci 2003, 21:199-212.
20. Cohen R., Kang A., Gulick C. Quantitative trait loci affecting the behavior of A/J and CBA/J intercross mice in the elevated plus maze. Mamm Genome 2001, 12:501-507.
21. Cole T.B., Walter B.J., Shih D.M., Tward A.D., Lusis A.J., Timchalk C., et al. Toxicity of chlorpyrifos and chlorpyrifos oxon in a transgenic mouse model of the human paraoxonase (PON1) Q192R polymorphism. Pharmacogenet Genomics 2005, 15:589-598.
22. Cruz-Morales S.E., Santos N.R., Brandao M.L. One-trial tolerance to midazolam is due to enhancement of fear and reduction of anxiolytic-sensitive behaviors in the elevated plus-maze retest in the rat. Pharmacol Biochem Behav 2002, 72:973-978.
23. Ducottet C., Belzung C. Correlations between behaviours in the elevated plus-maze and sensitivity to unpredictable subchronic mild stress: evidence from inbred strains of mice. Behav Brain Res 2005, 156:153-162.
24. Engel S.M., Berkowitz G.S., Barr D.B., Teitelbaum S.L., Siskind J., Meisel S.J., et al. Prenatal organophosphate metabolite and organochlorine levels and performance on the Brazelton Neonatal Behavioral Assessment Scale in a multiethnic pregnancy cohort. Am J Epidemiol 2007, 165:1397-1404.
25. Farchi N., Shoham S., Hochner B., Soreq H. Impaired hippocampal plasticity and errors in cognitive performance in mice with maladaptive AChE splice site selection. Eur J Neurosci 2007, 25:87-98.
26. File S.E., Gonzalez L.E., Andrews N. Endogenous acetylcholine in the dorsal hippocampus reduces anxiety through actions on nicotinic and muscarinic1 receptors. Behav Neurosci 1998, 112:352-359.
27. Furlong C.E., Holland N., Richter R.J., Bradman A., Ho A., Eskenazi B. PON1 status of farmworker mothers and children as a predictor of organophosphate sensitivity. Pharmacogenet Genomics 2006, 16:183-190.
28. Griebel G., Belzung C., Perrault G., Sanger D.J. Differences in anxiety-related behaviours and in sensitivity to diazepam in inbred and outbred strains of mice. Psychopharmacology (Berl) 2000, 148:164-170.
29. Guzzetti S., Calcagno E., Canetta A., Sacchetti G., Fracasso C., Caccia S., et al. Strain differences in paroxetine-induced reduction of immobility time in the forced swimming test in mice: role of serotonin. Eur J Pharmacol 2008, 594:117-124.
30. Haley R.W., Billecke S., La Du B.N. Association of low PON1 type Q (type A) arylesterase activity with neurologic symptom complexes in Gulf War veterans. Toxicol Appl Pharmacol 1999, 157:227-233.
31. Jacobson L.H., Cryan J.F. Feeling strained? Influence of genetic background on depression-related behavior in mice: a review. Behav Genet 2007, 37:171-213.
32. Jameson R.R., Seidler F.J., Slotkin T.A. Nonenzymatic functions of acetylcholinesterase splice variants in the developmental neurotoxicity of organophosphates: chlorpyrifos, chlorpyrifos oxon, and diazinon. Environ Health Perspect 2007, 115:65-70.
33. Kaufer D., Friedman A., Seidman S., Soreq H. Acute stress facilitates long-lasting changes in cholinergic gene expression. Nature 1998, 393:373-377.
34. Kofman O., Ben-Bashat G. Diisopropylfluorophosphate administration in the pre-weanling period induces long-term changes in anxiety behavior and passive avoidance in adult mice. Psychopharmacology (Berl) 2006, 183:452-461.
35. Kofman O., Shavit Y., Ashkenazi S., Gabay S. Habituation, discrimination and anxiety in transgenic mice overexpressing acetylcholinesterase splice variants. Brain Res 2007, 1185:170-178.
36. Lepicard E., Joubert C., Hagneau I., Perez-Diaz F., Chapouthier G. Differences in anxiety-related behavior and response to diazepam in BALB/cByJ and C57BL/6J strains of mice. Pharmacol Biochem Behav 2000, 67:739-748.
37. Levi Y., Kofman O., Schwebel M., Shaldubina A. Discrimination and avoidance learning in adult mice following developmental exposure to diisopropylfluorophosphate. Pharmacol Biochem Behav 2008, 88:438-445.
38. Lucki I., Dalvi A., Mayorga A.J. Sensitivity to the effects of pharmacologically selective antidepressants in different strains of mice. Psychopharmacology (Berl) 2001, 155:315-322.
39. McCobb D.P., Hara Y., Lai G.J., Mahmoud S.F., Flugge G. Subordination stress alters alternative splicing of the Slo gene in tree shrew adrenals. Horm Behav 2003, 43:180-186.
40. McNaughton N., Corr P.J. A two-dimensional neuropsychology of defense: fear/anxiety and defensive distance. Neurosci Biobehav Rev 2004, 28:285-305.
41. Meshorer E., Erb C., Gazit R., Pavlovsky L., Kaufer D., Friedman A., et al. Alternative splicing and neuritic mRNA translocation under long-term neuronal hypersensitivity. Science 2002, 295:508-512.
42. Milad M.R., Quirk G.J. Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 2002, 420:70-74.
43. Millstein R.A., Holmes A. Effects of repeated maternal separation on anxiety- and depression-related phenotypes in different mouse strains. Neurosci Biobehav Rev 2007, 31:3-17.
44. Mineur Y.S., Crusio W.E. Behavioral and neuroanatomical characterization of FVB/N inbred mice. Brain Res Bull 2002, 57:41-47.
45. Nijholt I., Farchi N., Kye M., Sklan E.H., Shoham S., Verbeure B., et al. Stress-induced alternative splicing of acetylcholinesterase results in enhanced fear memory and long-term potentiation. Mol Psychiatry 2004, 9:174-183.
46. Nikulina E.M., Skrinskaya J.A., Popova N.K. Role of genotype and dopamine receptors in behaviour of inbred mice in a forced swimming test. Psychopharmacology (Berl) 1991, 105:525-529.
47. Ofek K., Krabbe K.S., Evron T., Debecco M., Nielsen A.R., Brunnsgaad H., et al. Cholinergic status modulations in human volunteers under acute inflammation. J Mol Med 2007, 85:1239-1251.
48. Overstreet D.H., Janowsky D.S., Gillin J.C., Shiromani P.J., Sutin E.L. Stress-induced immobility in rats with cholinergic supersensitivity. Biol Psychiatry 1986, 21:657-664.
49. Perrier N.A., Salani M., Falasca C., Bon S., Augusti-Tocco G., Massoulie J. The readthrough variant of acetylcholinesterase remains very minor after heat shock, organophosphate inhibition and stress, in cell culture and in vivo. J Neurochem 2005, 94:629-638.
50. Petit-Demouliere B., Chenu F., Bourin M. Forced swimming test in mice: a review of antidepressant activity. Psychopharmacology (Berl) 2005, 177:245-255.
51. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29:e45.
52. Pugh P.L., Ahmed S.F., Smith M.I., Upton N., Hunter A.J. A behavioural characterisation of the FVB/N mouse strain. Behav Brain Res 2004, 155:283-289.
53. Rada P., Colasante C., Skirzewski M., Hernandez L., Hoebel B. Behavioral depression in the swim test causes a biphasic, long-lasting change in accumbens acetylcholine release, with partial compensation by acetylcholinesterase and muscarinic-1 receptors. Neuroscience 2006, 141:67-76.
54. Rogers D.C., Jones D.N., Nelson P.R., Jones C.M., Quilter C.A., Robinson T.L., et al. Use of SHIRPA and discriminant analysis to characterise marked differences in the behavioural phenotype of six inbred mouse strains. Behav Brain Res 1999, 105:207-217.
55. Roy V., Chapillon P., Jeljeli M., Caston J., Belzung C. Free versus forced exposure to an elevated plus-maze: evidence for new behavioral interpretations during test and retest. Psychopharmacology (Berl) 2009, 203:131-141.
56. Shanks N., Anisman H. Stressor-provoked behavioral changes in six strains of mice. Behav Neurosci 1988, 102:894-905.
57. Shohami E., Kaufer D., Chen Y., Seidman S., Cohen O., Ginzberg D., et al. Antisense prevention of neuronal damages following head injury in mice. J Mol Med 2000, 78:228-236.
58. Sklan E.H., Lowenthal A., Korner M., Ritov Y., Landers D.M., Rankinen T., et al. Acetylcholinesterase/paraoxonase genotype and expression predict anxiety scores in health, risk factors, exercise training, and genetics study. Proc Natl Acad Sci USA 2004, 101:5512-5517.
59. Slotkin T.A., Seidler F.J. Comparative developmental neurotoxicity of organophosphates in vivo: transcriptional responses of pathways for brain cell development, cell signaling, cytotoxicity and neurotransmitter systems. Brain Res Bull 2007, 72:232-274.
60. Soreq H., Seidman S. Acetylcholinesterase - new roles for an old actor. Nat Rev Neurosci 2001, 2:294-302.
61. StatSoft Inc (2008). STATISTICA (data analysis software system), version 8.0. http://www.statsoft.com/.
62. Sugimoto Y., Kajiwara Y., Hirano K., Yamada S., Tagawa N., Kobayashi Y., et al. Mouse strain differences in immobility and sensitivity to fluvoxamine and desipramine in the forced swimming test: analysis of serotonin and noradrenaline transporter binding. Eur J Pharmacol 2008, 592:116-122.
63. Trullas R., Skolnick P. Differences in fear motivated behaviors among inbred mouse strains. Psychopharmacology 1993, 111:323-331.
64. Wahlsten D., Metten P., Phillips T.J., Boehm S.L., Burkhart-Kasch S., Dorow J., et al. Different data from different labs: lessons from studies of gene-environment interaction. J Neurobiol 2003, 54:283-311.
65. Wehner J.M., Murphy-Erdsoh C., Smolen A., Smolen T.N. Genetic variation in paraoxonase activity and sensitivity to diisopropylphosphofluoridate in inbred mice. Pharmacol Biochem Behav 1987, 28:317-320.
66. Wong A.A., Brown R.E. Visual detection, pattern detection and visual acuity in 14 strains of mice. Genes, Brain Behav 2006, 5:389-403.
67. A, acetylcholine and serotonin receptors in the amygdala of seven inbred mouse strains. Behav Brain Res 2003, 145:145-159.
68. Yoshikawa T., Watanabe A., Ishitsuka Y., Nakaya A., Nakatani N. Identification of multiple genetic loci linked to the propensity for " behavioral despair" in mice. Genome Res 2002, 12:357-366.