Comt1 genotype and expression predicts anxiety and nociceptive sensitivity in inbred strains of mice

Genes, Brain and Behavior

Volumn 9, Issue 8, 2010, Pages 933-946

  Segall, S K ^a   Nackley, A G ^b   Diatchenko, L ^b   Lariviere, W R ^c   Lu, X ^b   Marron, J S ^b   Grabowski Boase, L ^d   Walker, J R ^d   Slade, G ^b,e   Gauthier, J ^b   Bailey, J S ^e   Steffy, B M ^f   Maynard, T M ^g   Tarantino, L M ^e   Wiltshire, T ^f  

^a Curriculum in Genetics and Molecular Biology   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d GENOMICS INSTITUTE OF THE NOVARTIS RESEARCH FOUNDATION   (United States)

^e Department of Dental Ecology ^*  (United States)

^f University of North Carolina   (United States)

^g UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Anxiety; B2 Sine; Behavior; COMT1; EQTL; Inbred mice; Pain

Indexed keywords

CATECHOL METHYLTRANSFERASE; COMPLEMENTARY DNA; MESSENGER RNA;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BEHAVIOR; BRAIN REGION; COMT1 GENE; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; GENOTYPE; HAPLOTYPE; INBRED STRAIN; MALE; MOUSE; MOUSE STRAIN; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; SHORT INTERSPERSED REPEAT;

ANIMALS; ANXIETY; CATECHOL O-METHYLTRANSFERASE; EXPLORATORY BEHAVIOR; FEMALE; HIPPOCAMPUS; MALE; MAZE LEARNING; MICE; MICE, INBRED STRAINS; MUTAGENESIS, INSERTIONAL; PAIN; PAIN THRESHOLD; RNA, MESSENGER; SPECIES SPECIFICITY;

ANIMALIA; MAMMALIA; MUS;

EID: 78349238506     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/j.1601-183X.2010.00633.x     Document Type: Article

References (61)

1. Andersen, S. & Skorpen, F. (2009) Variation in the COMT gene: implications for pain perception and pain treatment. Pharmacogenomics 10, 669-684.
2. Axelrod, J. & Tomchick, R. (1958) Enzymatic O-methylation of epinephrine and other catechols. J Biol Chem 233, 702-705.
3. Bailey, J.S., Grabowski-Boase, L., Steffy, B.M., Wiltshire, T., Churchill, G.A. & Tarantino, L.M. (2008) Identification of QTL for locomotor activation and anxiety using closely-related inbred strains. Genes Brain Behav 7, 761-769.
4. Benito, M., Parker, J., Du, Q., Wu, J., Xiang, D., Perou, C.M. & Marron, J.S. (2004) Adjustment of systematic microarray data biases. Bioinformatics 20, 105-114.
5. Chen, J., Lipska, B.K., Halim, N., Ma, Q.D., Matsumoto, M., Melhem, S., Kolachana, B.S., Hyde, T.M., Herman, M.M., Apud, J., Egan, M.F., Kleinman, J.E. & Weinberger, D.R. (2004) Functional analysis of genetic variation in catechol-O-methyltransferase (COMT): effects on mRNA, protein, and enzyme activity in postmortem human brain. Am J Hum Genet 75, 807-821.
6. Chen, Y., Zhu, J., Lum, P.Y. et al. (2008) Variations in DNA elucidate molecular networks that cause disease. Nature 452, 429-435.
7. Choleris, E., Thomas, A.W., Kavaliers, M. & Prato, F.S. (2001) A detailed ethological analysis of the mouse open field test: effects of diazepam, chlordiazepoxide and an extremely low frequency pulsed magnetic field. Neurosci Biobehav Rev 25, 235-260.
8. Crabbe, J.C., Gallaher, E.J., Cross, S.J. & Belknap, J.K. (1998) Genetic determinants of sensitivity to diazepam in inbred mice. Behav Neurosci 112, 668-677.
9. Crusio, W.E., Schwegler, H., Brust, I. & Van Abeelen, J.H. (1989a) Genetic selection for novelty-induced rearing behavior in mice produces changes in hippocampal mossy fiber distributions. J Neurogenet 5, 87-93.
10. Crusio, W.E., Schwegler, H. & Van Abeelen, J.H. (1989b) Behavioral responses to novelty and structural variation of the hippocampus in mice. I. Quantitative-genetic analysis of behavior in the open-field. Behav Brain Res 32, 75-80.
11. Czech, D.A., Jacobson, E.B., LeSueur-Reed, K.T. & Kazel, M.R. (2003) Putative anxiety-linked effects of the nitric oxide synthase inhibitor L-NAME in three murine exploratory behavior models. Pharmacol Biochem Behav 75, 741-748.
12. DeYoung, C.G., Getchell, M., Koposov, R.A., Yrigollen, C.M., Haeffel, G.J., Af Klinteberg, B., Oreland, L., Ruchkin, V.V., Pakstis, A.J. & Grigorenko, E.L. (2010) Variation in the catechol-O-methyltransferase Val 158 Met polymorphism associated with conduct disorder and ADHD symptoms, among adolescent male delinquents. Psychiatr Genet 20, 20-24.
13. Diatchenko, L., Slade, G.D., Nackley, A.G., Bhalang, K., Sigurdsson, A., Belfer, I., Goldman, D., Xu, K., Shabalina, S.A., Shagin, D., Max, M.B., Makarov, S.S. & Maixner, W. (2005) Genetic basis for individual variations in pain perception and the development of a chronic pain condition. Hum Mol Genet 14, 135-143.
14. Diatchenko, L., Nackley, A.G., Slade, G.D., Bhalang, K., Belfer, I., Max, M.B., Goldman, D. & Maixner, W. (2006a) Catechol-O-methyltransferase gene polymorphisms are associated with multiple pain-evoking stimuli. Pain 125, 216-224.
15. Diatchenko, L., Nackley, A.G., Slade, G.D., Fillingim, R.B. & Maixner, W. (2006b) Idiopathic pain disorders-pathways of vulnerability. Pain 123, 226-230.
16. Domschke, K., Freitag, C.M., Kuhlenbaumer, G., Schirmacher, A., Sand, P., Nyhuis, P., Jacob, C., Fritze, J., Franke, P., Rietschel, M., Garritsen, H.S., Fimmers, R., Nothen, M.M., Lesch, K.P., Stogbauer, F. & Deckert, J. (2004) Association of the functional V158M catechol-O-methyl-transferase polymorphism with panic disorder in women. Int J Neuropsychopharmacol 7, 183-188.
17. Domschke, K., Deckert, J., O'Donovan, M.C. & Glatt, S.J. (2007) Meta-analysis of COMT val158met in panic disorder: ethnic heterogeneity and gender specificity. Am J Med Genet B Neuropsychiatr Genet 144B, 667-673.
18. Eisener-Dorman, A.F., Grabowski-Boase, L., Steffy, B.M., Wiltshire, T. & Tarantino, L.M. (2010) Quantitative trait locus and haplotype mapping in closely related inbred strains identifies a locus for open field behavior. Mamm Genome 21, 231-246.
19. Eleftheriou, B.E. (1975) Regional brain catechol-O-methyl transferase: age related differences in the mouse. Exp Aging Res 1, 99-103.
20. Emin Erdal, M., Herken, H., Yilmaz, M. & Bayazit, Y.A. (2001) Significance of the catechol-O-methyltransferase gene polymorphism in migraine. Brain Res Mol Brain Res 94, 193-196.
21. Enoch, M.A., Xu, K., Ferro, E., Harris, C.R. & Goldman, D. (2003) Genetic origins of anxiety in women: a role for a functional catechol-O-methyltransferase polymorphism. Psychiatr Genet 13, 33-41.
22. Evans, J., Xu, K., Heron, J., Enoch, M.A., Araya, R., Lewis, G., Timpson, N., Davies, S., Nutt, D. & Goldman, D. (2009) Emotional symptoms in children: the effect of maternal depression, life events, and COMT genotype. Am J Med Genet B Neuropsychiatr Genet 150B, 209-218.
23. Fahey, J.M., Pritchard, G.A., Grassi, J.M., Pratt, J.S., Shader, R.I. & Greenblatt, D.J. (2001) Pharmacodynamic and receptor binding changes during chronic lorazepam administration. Pharmacol Biochem Behav 69, 1-8.
24. Fernandez, E.E. (1997) Structure of the mouse behaviour on the elevated plus-maze test of anxiety. Behav Brain Res 86, 105-112.
25. Frazer, K.A., Eskin, E., Kang, H.M., Bogue, M.A., Hinds, D.A., Beilharz, E.J., Gupta, R.V., Montgomery, J., Morenzoni, M.M., Nilsen, G.B., Pethiyagoda, C.L., Stuve, L.L., Johnson, F.M., Daly, M.J., Wade, C.M. & Cox, D.R. (2007) A sequence-based variation map of 8.27 million SNPs in inbred mouse strains. Nature 448, 1050-1053.
26. Fujita, O., Annen, Y. & Kitaoka, A. (1994) Tsukuba high- and low-emotional strains of rats (Rattus norvegicus): an overview. Behav Genet 24, 389-415.
27. Gogos, J.A., Morgan, M., Luine, V., Santha, M., Ogawa, S., Pfaff, D. & Karayiorgou, M. (1998) Catechol-O-methyltransferase-deficient mice exhibit sexually dimorphic changes in catecholamine levels and behavior. Proc Natl Acad Sci U S A 95, 9991-9996.
28. Gray, J. & McNaughton, N. (2000) The Neuropsychology of Anxiety. Oxford University Press, Oxford.
29. Guyton, A.C. (1991) In Wonsiewicz, M.J. (ed). Textbook of Medical Physiology. W.B. Saunders Company, Philadelphia, p. 676.
30. Harrison, P.J. & Tunbridge, E.M. (2008) Catechol-O-methyltransferase (COMT): a gene contributing to sex differences in brain function, and to sexual dimorphism in the predisposition to psychiatric disorders. Neuropsychopharmacology 33, 3037-3045.
31. Henderson, N.D., Turri, M.G., DeFries, J.C. & Flint, J. (2004) QTL analysis of multiple behavioral measures of anxiety in mice. Behav Genet 34, 267-293.
32. Hu, Z., Fan, C., Oh, D.S. et al. (2006) The molecular portraits of breast tumors are conserved across microarray platforms. BMC Genomics 7, 96.
33. Hughes, R.N. (1993) Effects on open-field behavior of diazepam and buspirone alone and in combination with chronic caffeine. Life Sci 53, 1217-1225.
34. Kabbaj, M., Devine, D.P., Savage, V.R. & Akil, H. (2000) Neurobiological correlates of individual differences in novelty-seeking behavior in the rat: differential expression of stress-related molecules. J Neurosci 20, 6983-6988.
35. Lachman, H.M. (2008) Does COMT val158met affect behavioral phenotypes: yes, no, maybe? Neuropsychopharmacology 33, 3027-3029.
36. Lang, U.E., Bajbouj, M., Sander, T. & Gallinat, J. (2007) Gender-dependent association of the functional catechol-O-methyltransferase Val158Met genotype with sensation seeking personality trait. Neuropsychopharmacology 32, 1950-1955.
37. Lariviere, W.R., Wilson, S.G., Laughlin, T.M., Kokayeff, A., West, E.E., Adhikari, S.M., Wan, Y. & Mogil, J.S. (2002) Heritability of nociception. III. Genetic relationships among commonly used assays of nociception and hypersensitivity. Pain 97, 75-86.
38. Lister, R.G. (1990) Ethologically-based animal models of anxiety disorders. Pharmacol Ther 46, 321-340.
39. Marron, J.S., Todd, M.J. & Ahn, J. (2007) Distance-weighted discrimination. J Am Stat Assoc 102, 1267-1271.
40. McClurg, P., Pletcher, M.T., Wiltshire, T. & Su, A.I. (2006) Comparative analysis of haplotype association mapping algorithms. BMC Bioinformatics 7, 61.
41. McClurg, P., Janes, J., Wu, C., Delano, D.L., Walker, J.R., Batalov, S., Takahashi, J.S., Shimomura, K., Kohsaka, A., Bass, J., Wiltshire, T. & Su, A.I. (2007) Genome wide association analysis in diverse inbred mice: power and population structure. Genetics 176, 675-683.
42. McCourt, W.F., Gurrera, R.J. & Cutter, H.S. (1993) Sensation seeking and novelty seeking. Are they the same? J Nerv Ment Dis 181, 309-312.
43. McNaughton, N. (1985) The effects of systemic and intraseptal injections of sodium amylobarbitone on rearing and ambulation in rats. Aust J Psychology 37, 15-27.
44. Mogil, J.S., Wilson, S.G., Bon, K., Lee, S.E., Chung, K., Raber, P., Pieper, J.O., Hain, H.S., Belknap, J.K., Hubert, L., Elmer, G.I., Chung, J.M. & Devor, M. (1999a) Heritability of nociception I: responses of 11 inbred mouse strains on 12 measures of nociception. Pain 80, 67-82.
45. Mogil, J.S., Wilson, S.G., Bon, K., Lee, S.E., Chung, K., Raber, P., Pieper, J.O., Hain, H.S., Belknap, J.K., Hubert, L., Elmer, G.I., Chung, J.M. & Devor, M. (1999b) Heritability of nociception II. 'Types' of nociception revealed by genetic correlation analysis. Pain 80, 83-93.
46. Nackley, A.G. & Diatchenko, L. (2010) Assessing potential functionality of catechol-O-methyltransferase (COMT) polymorphisms associated with pain sensitivity and temporomandibular joint disorders. Methods Mol Biol 617, 375-393.
47. Nackley, A.G., Shabalina, S.A., Tchivileva, I.E., Satterfield, K., Korchynskyi, O., Makarov, S.S., Maixner, W. & Diatchenko, L. (2006) Human catechol-O-methyltransferase haplotypes modulate protein expression by altering mRNA secondary structure. Science 314, 1930-1933.
48. Nackley, A.G., Tan, K.S., Fecho, K., Flood, P., Diatchenko, L. & Maixner, W. (2007) Catechol-O-methyltransferase inhibition increases pain sensitivity through activation of both beta2- and beta3-adrenergic receptors. Pain 128, 199-208.
49. Overbye, A. & Seglen, P.O. (2009) Phosphorylated and non-phosphorylated forms of catechol O-methyltransferase in rat liver, brain and other tissues. Biochem J 417, 535-545.
50. Palmason, H., Moser, D., Sigmund, J., Vogler, C., Hanig, S., Schneider, A., Seitz, C., Marcus, A., Meyer, J. & Freitag, C.M. (2009) Attention-deficit/hyperactivity disorder phenotype is influenced by a functional catechol-O-methyltransferase variant. J Neural Transm 117, 259-267.
51. Papaleo, F., Crawley, J.N., Song, J., Lipska, B.K., Pickel, J., Weinberger, D.R. & Chen, J. (2008) Genetic dissection of the role of catechol-O-methyltransferase in cognition and stress reactivity in mice. J Neurosci 28, 8709-8723.
52. Piazza, P.V., Deminiere, J.M., Le Moal, M. & Simon, H. (1989) Factors that predict individual vulnerability to amphetamine self-administration. Science 245, 1511-1513.
53. Pletcher, M.T., McClurg, P., Batalov, S., Su, A.I., Barnes, S.W., Lagler, E., Korstanje, R., Wang, X., Nusskern, D., Bogue, M.A., Mural, R.J., Paigen, B. & Wiltshire, T. (2004) Use of a dense single nucleotide polymorphism map for in silico mapping in the mouse. PLoS Biol 2, e393.
54. Pooley, E.C., Fineberg, N. & Harrison, P.J. (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.
55. Qian, Q., Wang, Y., Zhou, R., Li, J., Wang, B., Glatt, S. & Faraone, S.V. (2003) Family-based and case-control association studies of catechol-O-methyltransferase in attention deficit hyperactivity disorder suggest genetic sexual dimorphism. Am J Med Genet B Neuropsychiatr Genet 118B, 103-109.
56. Stein, M.B., Fallin, M.D., Schork, N.J. & Gelernter, J. (2005) COMT polymorphisms and anxiety-related personality traits. Neuropsychopharmacology 30, 2092-2102.
57. Su, A.I., Wiltshire, T., Batalov, S., Lapp, H., Ching, K.A., Block, D., Zhang, J., Soden, R., Hayakawa, M., Kreiman, G., Cooke, M.P., Walker, J.R. & Hogenesch, J.B. (2004) A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci U S A 101, 6062-6067.
58. Vlainic, J. & Pericic, D. (2009) Effects of acute and repeated zolpidem treatment on pentylenetetrazole-induced seizure threshold and on locomotor activity: comparison with diazepam. Neuropharmacology 56, 1124-1130.
59. Wu, C., Delano, D.L., Mitro, N., Su, S.V., Janes, J., McClurg, P., Batalov, S., Welch, G.L., Zhang, J., Orth, A.P., Walker, J.R., Glynne, R.J., Cooke, M.P., Takahashi, J.S., Shimomura, K., Kohsaka, A., Bass, J., Saez, E., Wiltshire, T. & Su, A.I. (2008) Gene set enrichment in eQTL data identifies novel annotations and pathway regulators. PLoS Genet 4, e1000070.
60. Yang, H., Bell, T.A., Churchill, G.A. & Pardo-Manuel de Villena, F. (2007) On the subspecific origin of the laboratory mouse. Nat Genet 39, 1100-1107.
61. Zubieta, J.K., Heitzeg, M.M., Smith, Y.R., Bueller, J.A., Xu, K., Xu, Y., Koeppe, R.A., Stohler, C.S. & Goldman, D. (2003) COMT val158met genotype affects mu-opioid neurotransmitter responses to a pain stressor. Science 299, 1240-1243.