Genotype-Dependent Effects of COMT Inhibition on Cognitive Function in a Highly Specific, Novel Mouse Model of Altered COMT Activity

Neuropsychopharmacology

Volumn 41, Issue 13, 2016, Pages 3060-3069

  Barkus, Chris ^a   Korn, Clio ^a   Stumpenhorst, Katharina ^a   Laatikainen, Linda M ^a   Ballard, Dominic ^b   Lee, Sheena ^c   Sharp, Trevor ^c   Harrison, Paul J ^a,d   Bannerman, David M ^c   Weinberger, Daniel R ^e   Chen, Jingshan ^f   Tunbridge, Elizabeth M ^a,d  

^a WARNEFORD HOSPITAL   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d OXFORD HEALTH NHS FOUNDATION TRUST   (United Kingdom)

^e JOHNS HOPKINS UNIVERSITY   (United States)

^f NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3,4 DIHYDROXYPHENYLACETIC ACID; CATECHOL METHYLTRANSFERASE; HOMOVANILLIC ACID; TOLCAPONE; BENZOPHENONE DERIVATIVE; CATECHOL METHYLTRANSFERASE INHIBITOR; COMT PROTEIN, MOUSE; METHIONINE; NITROPHENOL; VALINE;

ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; CHROMOSOME DELETION 22Q11; COGNITION; CONTROLLED STUDY; DOPAMINE METABOLISM; DORSAL HIPPOCAMPUS; DORSAL STRIATUM; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; FRONTAL CORTEX; GENE EXPRESSION; GENOTYPE; HOMOZYGOTE; LEARNING; MALE; MEMORY; MOUSE; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; REACTION TIME; TRANSGENE; VENTRAL HIPPOCAMPUS; ANALYSIS OF VARIANCE; ANIMAL; BRAIN; COGNITION DISORDERS; DECISION MAKING; DISEASE MODEL; DRUG EFFECTS; EXPLORATORY BEHAVIOR; GENETICS; MAZE TEST; METABOLISM; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSGENIC MOUSE;

ANALYSIS OF VARIANCE; ANIMALS; BENZOPHENONES; BRAIN; CATECHOL O-METHYLTRANSFERASE; CATECHOL O-METHYLTRANSFERASE INHIBITORS; CHOICE BEHAVIOR; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; EXPLORATORY BEHAVIOR; GENOTYPE; MAZE LEARNING; METHIONINE; MICE; MICE, TRANSGENIC; NITROPHENOLS; POLYMORPHISM, SINGLE NUCLEOTIDE; REACTION TIME; VALINE;

EID: 84981172870     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2016.119     Document Type: Article

References (55)

1. Apud JA, Mattay V, Chen J, Kolachana BS, Callicott JH, Rasetti R et al (2007). Tolcapone improves cognition and cortical information processing in normal human subjects. Neuropsychopharmacology 32: 1011-1020.
2. Babovic D, O'Tuathaigh CM, O'Connor AM, O'Sullivan GJ, Tighe O, Croke DT et al (2008). Phenotypic characterization of cognition and social behavior in mice with heterozygous versus homozygous deletion of catechol-O-methyltransferase. Neuroscience 155: 1021-1029.
3. Bari A, Dalley JW, Robbins TW (2008). The application of the 5-choice serial reaction time task for the assessment of visual attentional processes and impulse control in rats. Nat Protocols 3: 759-767.
4. Barkus C, Dawson LA, Sharp T, Bannerman DM (2012). GluN1 hypomorph mice exhibit wide-ranging behavioral alterations. Genes Brain Behav 11: 342-351.
5. Baumann C, Klauke B, Weber H, Domschke K, Zwanzger P, Pauli P et al (2013). The interaction of early life experiences with COMT val158met affects anxiety sensitivity. Genes Brain Behav 12: 821-829.
6. Caspi A, Moffitt TE, Cannon M, McClay J, Murray R, Harrington H et al (2005). Moderation of the effect of adolescent-onset cannabis use on adult psychosis by a functional polymorphism in the catechol-O-methyltransferase gene: longitudinal evidence of a gene X environment interaction. Biol Psychiatry 57: 1117-1127.
7. Chen J, Lipska BK, Halim N, Ma QD, Matsumoto M, Melhem S et al (2004). Functional analysis of genetic variation in catechol-O-methyltransferase (COMT): effects on mRNA, protein, enzyme activity in postmortem human brain. Am J Hum Genet 75: 807-821.
8. Chudasama Y, Robbins TW (2004). Psychopharmacological approaches to modulating attention in the five-choice serial reaction time task: implications for schizophrenia. Psychopharmacol (Berl) 174: 86-98.
9. Desbonnet L, Tighe O, Karayiorgou M, Gogos JA, Waddington JL, O'Tuathaigh CM (2012). Physiological and behavioural responsivity to stress and anxiogenic stimuli in COMT-deficient mice. Behav Brain Res 228: 351-358.
10. Drew LJ, Crabtree GW, Markx S, Stark KL, Chaverneff F, Xu B et al (2011). The 22q11. 2 microdeletion: fifteen years of insights into the genetic and neural complexity of psychiatric disorders. Int J Devl Neurosci 29: 259-281.
11. Egan MF, Goldberg TE, Kolachana BS, Callicott JH, Mazzanti CM, Straub RE et al (2001). Effect of COMT Val108/158 Met genotype on frontal lobe function and risk for schizophrenia. Proc Natl Acad Sci USA 98: 6917-6922.
12. Enoch MA, Xu K, Ferro E, Harris CR, Goldman D (2003). Genetic origins of anxiety in women: a role for a functional catechol-Omethyltransferase polymorphism. Psychiatr Genet 13: 33-41.
13. Farrell MS, Werge T, Sklar P, Owen MJ, Ophoff RA, O'Donovan MC et al (2015). Evaluating historical candidate genes for schizophrenia. Mol Psychiatry 20: 555-562.
14. Farrell SM, Tunbridge EM, Braeutigam S, Harrison PJ (2012). COMT Val(158)Met genotype determines the direction of cognitive effects produced by catechol-O-methyltransferase inhibition. Biol Psychiatry 71: 538-544.
15. Giakoumaki SG, Roussos P, Bitsios P (2008). Improvement of prepulse inhibition and executive function by the COMT inhibitor tolcapone depends on COMT Val158Met polymorphism. Neuropsychopharmacology 33: 3058-3068.
16. Gogos JA, Morgan M, Luine V, Santha M, Ogawa S, Pfaff D et al (1998). Catechol-O-methyltransferase-deficient mice exhibit sexually dimorphic changes in catecholamine levels and behavior. Proc Natl Acad Sci USA 95: 9991-9996.
17. Goldman-Rakic PS, Muly EC 3rd, Williams GV (2000). D(1) receptors in prefrontal cells and circuits. Brain Res Brain Res Rev 31: 295-301.
18. Gothelf D, Law AJ, Frisch A, Chen J, Zarchi O, Michaelovsky E et al (2014). Biological effects of COMT haplotypes and psychosis risk in 22q11. 2 deletion syndrome. Biol Psychiatry 75: 406-413.
19. Grissom NM, Herdt CT, Desilets J, Lidsky-Everson J, Reyes TM (2015). Dissociable deficits of executive function caused by gestational adversity are linked to specific transcriptional changes in the prefrontal cortex. Neuropsychopharmacology 40: 1353-1363.
20. Hertel P, Mathe JM, Nomikos GG, Iurlo M, Mathe AA, Svensson TH (1995). Effects of D-amphetamine and phencyclidine on behavior and extracellular concentrations of neurotensin and dopamine in the ventral striatum and the medial prefrontal cortex of the rat. Behav Brain Res 72: 103-114.
21. Huotari M, Gainetdinov R, Mannisto PT (1999). Microdialysis studies on the action of tolcapone on pharmacologically-elevated extracellular dopamine levels in conscious rats. Pharmacol Toxicol 85: 233-238.
22. Kaenmaki M, Tammimaki A, Myohanen T, Pakarinen K, Amberg C, Karayiorgou M et al (2010). Quantitative role of COMT in dopamine clearance in the prefrontal cortex of freely moving mice. J Neurochem 114: 1745-1755.
23. Karayiorgou M, Simon TJ, Gogos JA (2010). 22q11. 2 Microdeletions: linking DNA structural variation to brain dysfunction and schizophrenia. Nat Rev Neurosci 11: 402-416.
24. Konishi Y, Tanii H, Otowa T, Sasaki T, Tochigi M, Umekage T et al (2014). Genexgenexgender interaction of BDNF and COMT genotypes associated with panic disorder. Progr Neuropsychopharmacol Biol Psychiatry 51: 119-125.
25. Laatikainen LM, Sharp T, Bannerman DM, Harrison PJ, Tunbridge EM (2012). Modulation of hippocampal dopamine metabolism and hippocampal-dependent cognitive function by catechol-O-methyltransferase inhibition. J Psychopharmacol 26: 1561-1568.
26. Lapish CC, Ahn S, Evangelista LM, So K, Seamans JK, Phillips AG (2009). Tolcapone enhances food-evoked dopamine efflux and executive memory processes mediated by the rat prefrontal cortex. Psychopharmacology (Berl) 202: 521-530.
27. Lee LO, Prescott CA (2014). Association of the catechol-Omethyltransferase val158met polymorphism and anxiety-related traits: a meta-analysis. Psychiatr Genet 24: 52-69.
28. Lotta T, Vidgren J, Tilgmann C, Ulmanen I, Melen K, Julkunen I et al (1995). Kinetics of human soluble and membrane-bound catechol O-methyltransferase: a revised mechanism and description of the thermolabile variant of the enzyme. Biochemistry 34: 4202-4210.
29. Lusis AJ, Yu J, Wang SS (2007). The problem of passenger genes in transgenic mice. Arterioscler Thromb Vasc Biol 27: 2100-2103.
30. Mattay VS, Goldberg TE, Fera F, Hariri AR, Tessitore A, Egan MF et al (2003). Catechol O-methyltransferase val158-met genotype and individual variation in the brain response to amphetamine. Proc Natl Acad Sci USA 100: 6186-6191.
31. Meyer-Lindenberg A, Nichols T, Callicott JH, Ding J, Kolachana B, Buckholtz J et al (2006). COMT haplotype variation affects human prefrontal function. Mol Psychiatry 11: 797.
32. Nackley AG, Shabalina SA, Tchivileva IE, Satterfield K, Korchynskyi O, Makarov SS et al (2006). Human catechol-O-methyltransferase haplotypes modulate protein expression by altering mRNA secondary structure. Science 314: 1930-1933.
33. Niarchou M, Zammit S, Escott-Price V, Owen MJ, van den Bree MB (2014). Exploring the indirect effects of catechol-O-methyltransferase (COMT) genotype on psychotic experiences through cognitive function and anxiety disorders in a large birth cohort of children. Am J Med Genet B 165B: 410-420.
34. Olson EN, Arnold HH, Rigby PW, Wold BJ (1996). Know your neighbors: three phenotypes in null mutants of the myogenic bHLH gene MRF4. Cell 85: 1-4.
35. Olsson CA, Anney RJ, Lotfi-Miri M, Byrnes GB, Williamson R, Patton GC (2005). Association between the COMT Val158Met polymorphism and propensity to anxiety in an Australian population-based longitudinal study of adolescent health. Psychiatr Genet 15: 109-115.
36. Palmatier MA, Kang AM, Kidd KK (1999). Global variation in the frequencies of functionally different catechol-O-methyltransferase alleles. Biol Psychiatry 46: 557-567.
37. Papaleo F, Crawley JN, Song J, Lipska BK, Pickel J, Weinberger DR et al (2008). Genetic dissection of the role of catechol-Omethyltransferase in cognition and stress reactivity in mice. J Neurosci 28: 8709-8723.
38. Papaleo F, Erickson L, Liu G, Chen J, Weinberger DR (2012). Effects of sex and COMT genotype on environmentally modulated cognitive control in mice. Proc Natl Acad Sci USA 109: 20160-20165.
39. Paterlini M, Zakharenko SS, Lai WS, Qin J, Zhang H, Mukai J et al (2005). Transcriptional and behavioral interaction between 22q11. 2 orthologs modulates schizophrenia-related phenotypes in mice. Nat Neurosci 8: 1586-1594.
40. Paterson NE, Ricciardi J, Wetzler C, Hanania T (2011). Sub-optimal performance in the 5-choice serial reaction time task in rats was sensitive to methylphenidate, atomoxetine and d-amphetamine, but unaffected by the COMT inhibitor tolcapone. Neurosci Res 69: 41-50.
41. Pooley EC, Fineberg N, Harrison PJ (2007). The met(158) allele of catechol-O-methyltransferase (COMT) is associated with obsessive-compulsive disorder in men: case-control study and meta-analysis. Mol Psychiatry 12: 556-561.
42. Reisel D, Bannerman DM, Schmitt WB, Deacon RM, Flint J, Borchardt T et al (2002). Spatial memory dissociations in mice lacking GluR1. Nat Neurosci 5: 868-873.
43. Risbrough V, Ji B, Hauger R, Zhou X (2014). Generation and characterization of humanized mice carrying COMT158 Met/Val alleles. Neuropsychopharmacology 39: 1823-1832.
44. Robinson RG, Smith SM, Wolkenberg SE, Kandebo M, Yao L, Gibson CR et al (2012). Characterization of non-nitrocatechol pan and isoform specific catechol-O-methyltransferase inhibitors and substrates. ACS Chem Neurosci 3: 129-140.
45. Scheggia D, Bebensee A, Weinberger DR, Papaleo F (2014). The ultimate intra-/extra-dimensional attentional set-shifting task for mice. Biol Psychiatry 75: 660-670.
46. Simpson EH, Morud J, Winiger V, Biezonski D, Zhu JP, Bach ME et al (2014). Genetic variation in COMT activity impacts learning and dopamine release capacity in the striatum. Learn Mem 21: 205-214.
47. Tan HY, Chen Q, Sust S, Buckholtz JW, Meyers JD, Egan MF et al (2007). Epistasis between catechol-O-methyltransferase and type II metabotropic glutamate receptor 3 genes on working memory brain function. Proc Natl Acad Sci USA 104: 12536-12541.
48. Tunbridge EM, Bannerman DM, Sharp T, Harrison PJ (2004). Catechol-O-methyltransferase inhibition improves set-shifting performance and elevates stimulated dopamine release in the rat prefrontal cortex. J Neurosci 24: 5331-5335.
49. Tunbridge EM, Harrison PJ (2011). Importance of the COMT gene for sex differences in brain function and predisposition to psychiatric disorders. Curr Top Behav Neurosci 8: 119-140.
50. Tunbridge EM, Harrison PJ, Weinberger DR (2006). Catechol-Omethyltransferase, cognition, psychosis: Val158Met and beyond. Biol Psychiatry 60: 141-151.
51. Tunbridge EM, Huber A, Farrell SM, Stumpenhorst K, Harrison PJ, Walton ME (2012). The role of catechol-O-methyltransferase in reward processing and addiction. CNS Neurol Disord Drug Targets 11: 306-323.
52. Ursini G, Bollati V, Fazio L, Porcelli A, Iacovelli L, Catalani A et al (2011). Stress-related methylation of the catechol-O-methyltransferase Val 158 allele predicts human prefrontal cognition and activity. J Neurosci 31: 6692-6698.
53. von Engelhardt J, Doganci B, Jensen V, Hvalby O, Gongrich C, Taylor A et al (2008). Contribution of hippocampal and extrahippocampal NR2B-containing NMDA receptors to performance on spatial learning tasks. Neuron 60: 846-860.
54. Woo JM, Yoon KS, Yu BH (2002). Catechol O-methyltransferase genetic polymorphism in panic disorder. Am J Psychiatry 159: 1785-1787.
55. Yavich L, Forsberg MM, Karayiorgou M, Gogos JA, Mannisto PT (2007). Site-specific role of catechol-O-methyltransferase in dopamine overflow within prefrontal cortex and dorsal striatum. J Neurosci 27: 10196-10209.