Social deficits and perseverative behaviors, but not overt aggression, in MAO-A hypomorphic mice

Neuropsychopharmacology

Volumn 36, Issue 13, 2011, Pages 2674-2688

  Bortolato, Marco ^a   Chen, Kevin ^a   Godar, Sean C ^a   Chen, Gao ^a   Wu, Weihua ^a   Rebrin, Igor ^a   Farrell, Mollee R ^b   Scott, Anna L ^a   Wellman, Cara L ^b   Shih, Jean C ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b INDIANA UNIVERSITY   (United States)

Author keywords

aggression; anxiety; monoamine oxidase A; repetitive behaviors; social interaction; transgenic mice

Indexed keywords

AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME A; NEOMYCIN; NORADRENALIN; SEROTONIN;

AGGRESSION; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CELL SIZE; CONTROLLED STUDY; DENDRITE; ENZYME DEFICIENCY; ENZYME METABOLISM; EXPERIMENTAL TEST; GENE CASSETTE; GENE INSERTION; GENETIC TRANSCRIPTION; GENOTYPE; HIPPOCAMPUS; INTRON; MALE; MESENCEPHALON; MOLECULAR CLONING; MORPHOLOGY; MOUSE; NEUROCHEMISTRY; NONHUMAN; OPEN FIELD BEHAVIOR; ORBITAL CORTEX; OVERT AGGRESSION; PERSEVERATION; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN POLYMORPHISM; REAL TIME POLYMERASE CHAIN REACTION; SOCIAL INTERACTION; SOCIAL ISOLATION;

AGGRESSION; ANIMALS; BEHAVIOR, ANIMAL; DENDRITES; DISEASE MODELS, ANIMAL; FRONTAL LOBE; HUMANS; MALE; MENTAL DISORDERS; MICE; MICE, 129 STRAIN; MICE, KNOCKOUT; MICE, NEUROLOGIC MUTANTS; MONOAMINE OXIDASE; PYRAMIDAL CELLS; SOCIAL BEHAVIOR; STEREOTYPED BEHAVIOR;

EID: 80855123827     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2011.157     Document Type: Article

References (81)

1. Alia-Klein N, Goldstein RZ, Kriplani A, Logan J, Tomasi D, Williams B et al (2008). Brain monoamine oxidase A activity predicts trait aggression. J Neurosci 28: 5099-5104.
2. Alptekin K, Degirmenci B, Kivircik B, Durak H, Yemez B, Derebek E et al (2001). Tc-99 m HMPAO brain perfusion SPECT in drug-free obsessive-compulsive patients without depression. Psychiatry Res 107: 51-56. (Pubitemid 32706506)
3. Bach AW, Lan NC, Johnson DL, Abell CW, Bembenek ME, Kwan SW et al (1988). cDNA cloning of human liver monoamine oxidase A and B: molecular basis of differences in enzymatic properties. Proc Natl Acad Sci USA 85: 4934-4938.
4. Barrow JR, Capecchi MR (1996). Targeted disruption of the Hoxb-2 locus in mice interferes with expression of Hoxb-1 and Hoxb-4. Development 122: 3817-3828. (Pubitemid 27033878)
5. Battaglia M, Ogliari A (2005). Anxiety and panic: from human studies to animal research and back. Neurosci Biobehav Rev 29: 169-179. (Pubitemid 40094586)
6. Bortolato M, Chen K, Shih JC (2008). Monoamine oxidase inactivation: from pathophysiology to therapeutics. Adv Drug Deliv Rev 60: 1527-1533.
7. Bortolato M, Frau R, Orru M, Piras AP, Fa M, Tuveri A et al (2007). Activation of GABA(B) receptors reverses spontaneous gating deficits in juvenile DBA/2J mice. Psychopharmacology 194: 361-369. (Pubitemid 47389346)
8. Brummett BH, Boyle SH, Siegler IC, Kuhn CM, Surwit RS, Garrett ME et al (2008). HPA axis function in male caregivers: effect of the monoamine oxidase-A gene promoter (MAOA-uVNTR). Biol Psychol 79: 250-255.
9. Brunner HG, Nelen M, Breakefield XO, Ropers HH, van Oost BA (1993). Abnormal behavior associated with a point mutation in the structural gene for monoamine oxidase A. Science 262: 578-580. (Pubitemid 23350673)
10. Buckholtz JW, Callicott JH, Kolachana B, Hariri AR, Goldberg TE, Genderson M et al (2008). Genetic variation in MAOA modulates ventromedial prefrontal circuitry mediating individual differences in human personality. Mol Psychiatry 13: 313-324. (Pubitemid 351272649)
11. Buckholtz JW, Meyer-Lindenberg A (2008). MAOA and the neurogenetic architecture of human aggression. Trends Neurosci 31: 120-129.
12. Buell SJ (1982). Golgi-Cox and rapid Golgi methods as applied to autopsied human brain tissue: widely disparate results. J Neuropathol Exp Neurol 41: 500-507. (Pubitemid 12033254)
13. Camarena B, Rinetti G, Cruz C, Gomez A, de La Fuente JR, Nicolini H (2001). Additional evidence that genetic variation of MAO-A gene supports a gender subtype in obsessive-compulsive disorder. Am J Med Genet 105: 279-282. (Pubitemid 32410903)
14. Cases O, Seif I, Grimsby J, Gaspar P, Chen K, Pournin S et al (1995). Aggressive behavior and altered amounts of brain serotonin and norepinephrine in mice lacking MAOA. Science 268: 1763-1766.
15. Caspi A, McClay J, Moffitt TE, Mill J, Martin J, Craig IW et al (2002). Role of genotype in the cycle of violence in maltreated children. Science 297: 851-854. (Pubitemid 34839638)
16. Cerasa A, Cherubini A, Quattrone A, Gioia MC, Magariello A, Muglia M et al (2010). Morphological correlates of MAO A VNTR polymorphism: new evidence from cortical thickness measurement. Behav Brain Res 211: 118-124.
17. Cerasa A, Gioia MC, Labate A, Lanza P, Magariello A, Muglia M et al (2008). MAO A VNTR polymorphism and variation in human morphology: a VBM study. Neuroreport 19: 1107-1110.
18. Chen K, Cases O, Rebrin I, Wu W, Gallaher TK, Seif I et al (2007). Forebrain-specific expression of monoamine oxidase A reduces neurotransmitter levels, restores the brain structure, and rescues aggressive behavior in monoamine oxidase A-deficient mice. J Biol Chem 282: 115-123. (Pubitemid 47076592)
19. Cohen IL, Liu X, Lewis ME, Chudley A, Forster-Gibson C, Gonzalez M et al (2011). Autism severity is associated with child and maternal MAOA genotypes. Clin Genet 79: 355-362.
20. Coleman PD, Flood DG (1987). Neuron numbers and dendritic extent in normal aging and Alzheimer's disease. Neurobiol Aging 8: 521-545. (Pubitemid 18006178)
21. Crawley JN (2000). What's Wrong with My Mouse 1st edn. Wiley-Liss: New York.
22. De Colibus L, Li M, Binda C, Lustig A, Edmondson DE, Mattevi A (2005). Three-dimensional structure of human monoamine oxidase A (MAO A): relation to the structures of rat MAO A and human MAO B. Proc Natl Acad Sci USA 102: 12684-12689. (Pubitemid 41279426)
23. Denys D, van der Wee N, Janssen J, De Geus F, Westenberg HG (2004). Low level of dopaminergic D2 receptor binding in obsessive-compulsive disorder. Biol Psychiatry 55: 1041-1045. (Pubitemid 38581920)
24. Dijkhuizen PA, Ghosh A (2005). Regulation of dendritic growth by calcium and neurotrophin signaling. Prog Brain Res 147: 17-27.
25. Durig J, Hornung JP (2000). Neonatal serotonin depletion affects developing and mature mouse cortical neurons. Neuroreport 11: 833-837. (Pubitemid 30173933)
26. Fineberg NA, Potenza MN, Chamberlain SR, Berlin HA, Menzies L, Bechara A et al (2010). Probing compulsive and impulsive behaviors, from animal models to endophenotypes: a narrative review. Neuropsychopharmacology 35: 591-604.
27. Gallo G, Letourneau PC (1998). Axon guidance: GTPases help axons reach their targets. Curr Biol 8: R80-R82. (Pubitemid 28091562)
28. Garrett JE, Wellman CL (2009). Chronic stress effects on dendritic morphology in medial prefrontal cortex: sex differences and estrogen dependence. Neuroscience 162: 195-207.
29. Gattoni R, Mahe D, Mahl P, Fischer N, Mattei MG, Stevenin J et al (1996). The human hnRNP-M proteins: structure and relation with early heat shock-induced splicing arrest and chromosome mapping. Nucleic Acids Res 24: 2535-2542. (Pubitemid 26237152)
30. Glaser EM, Van der Loos H (1981). Analysis of thick brain sections by obverse-reverse computer microscopy: application of a new, high clarity Golgi-Nissl stain. J Neurosci Methods 4: 117-125. (Pubitemid 11005370)
31. Godar SC, Bortolato M, Frau R, Dousti M, Chen K, Shih JC (2010). Maladaptive defensive behaviours in monoamine oxidase A-deficient mice. Int J Neuropsychopharmacol 15: 1-13.
32. Graybiel AM, Rauch SL (2000). Toward a neurobiology of obsessive-compulsive disorder. Neuron 28: 343-347.
33. Grimsby J, Toth M, Chen K, Kumazawa T, Klaidman L, Adams JD et al (1997). Increased stress response and beta-phenylethyla-mine in MAOB-deficient mice. Nat Genet 17: 206-210.
34. Jacob CP, Muller J, Schmidt M, Hohenberger K, Gutknecht L, Reif A et al (2005). Cluster B personality disorders are associated with allelic variation of monoamine oxidase A activity. Neuropsychopharmacology 30: 1711-1718. (Pubitemid 43086028)
35. Kim-Cohen J, Caspi A, Taylor A, Williams B, Newcombe R, Craig IW et al (2006). MAOA, maltreatment, and gene-environment interaction predicting children's mental health: new evidence and a meta-analysis. Mol Psychiatry 11: 903-913. (Pubitemid 44470213)
36. Kontis D, Boulougouris V, Papakosta VM, Kalogerakou S, Papadopoulos S, Poulopoulou C et al (2008). Dopaminergic and serotonergic modulation of persistent behaviour in the reinforced spatial alternation model of obsessive-compulsive disorder. Psychopharmacology 200: 597-610.
37. Kwon HB, Sabatini BL (2011). Glutamate induces de novo growth of functional spines in developing cortex. Nature 474: 100-104.
38. Lacerda AL, Hardan AY, Yorbik O, Keshavan MS (2003). Measurement of the orbitofrontal cortex: a validation study of a new method. Neuroimage 19: 665-673. (Pubitemid 36918211)
39. Lai GJ, McCobb DP (2006). Regulation of alternative splicing of Slo K+ channels in adrenal and pituitary during the stress-hyporesponsive period of rat development. Endocrinology 147: 3961-3967. (Pubitemid 44079402)
40. Lan NC, Heinzmann C, Gal A, Klisak I, Orth U, Lai E et al (1989). Human monoamine oxidase A and B genes map to Xp 11.23 and are deleted in a patient with Norrie disease. Genomics 4: 552-559.
41. Lee BT, Ham BJ (2008). Monoamine oxidase A-uVNTR genotype affects limbic brain activity in response to affective facial stimuli. Neuroreport 19: 515-519.
42. Lewandoski M (2001). Conditional control of gene expression in the mouse. Nat Rev Genet 2: 743-755. (Pubitemid 33685572)
43. Lieske V, Bennett-Clarke CA, Rhoades RW (1999). Effects of serotonin on neurite outgrowth from thalamic neurons in vitro. Neuroscience 90: 967-974. (Pubitemid 29156761)
44. Ma J, Yoshimura M, Yamashita E, Nakagawa A, Ito A, Tsukihara T (2004). Structure of rat monoamine oxidase A and its specific recognitions for substrates and inhibitors. J Mol Biol 338: 103-114. (Pubitemid 38429789)
45. Maas JW (1962). Neurochemical differences between two strains of mice. Science 137: 621-622.
46. Manuck SB, Flory JD, Ferrell RE, Mann JJ, Muldoon MF (2000). A regulatory polymorphism of the monoamine oxidase-A gene may be associated with variability in aggression, impulsivity, and central nervous system serotonergic responsivity. Psychiatry Res 95: 9-23. (Pubitemid 30445200)
47. McGrath MJ, Campbell KM, Veldman MB, Burton FH (1999). Anxiety in a transgenic mouse model of cortical-limbic neuro-potentiated compulsive behavior. Behav Pharmacol 10: 435-443. (Pubitemid 29440551)
48. Meerson A, Cacheaux L, Goosens KA, Sapolsky RM, Soreq H, Kaufer D (2010). Changes in brain microRNAs contribute to cholinergic stress reactions. J Mol Neurosci 40: 47-55.
49. Mejia JM, Ervin FR, Baker GB, Palmour RM (2002). Monoamine oxidase inhibition during brain development induces pathological aggressive behavior in mice. Biol Psychiatry 52: 811-821.
50. Meshorer E, Bryk B, Toiber D, Cohen J, Podoly E, Dori A et al (2005). SC35 promotes sustainable stress-induced alternative splicing of neuronal acetylcholinesterase mRNA. Mol Psychiatry 10: 985-997. (Pubitemid 41541984)
51. Meyer-Lindenberg A, Buckholtz JW, Kolachana B, A RH, Pezawas L, Blasi G et al (2006). Neural mechanisms of genetic risk for impulsivity and violence in humans. Proc Natl Acad Sci USA 103: 6269-6274.
52. Micallef J, Blin O (2001). Neurobiology and clinical pharmacology of obsessive-compulsive disorder. Clin Neuropharmacol 24: 191-207. (Pubitemid 32717853)
53. Mohn AR, Gainetdinov RR, Caron MG, Koller BH (1999). Mice with reduced NMDA receptor expression display behaviors related to schizophrenia. Cell 98: 427-436. (Pubitemid 29402481)
54. Nagy A, Moens C, Ivanyi E, Pawling J, Gertsenstein M, Hadjantonakis AK et al (1998). Dissecting the role of N-myc in development using a single targeting vector to generate a series of alleles. Curr Biol 8: 661-664. (Pubitemid 28257971)
55. Oreland L, Nilsson K, Damberg M, Hallman J (2007). Monoamine oxidases: activities, genotypes and the shaping of behaviour. J Neural Transm 114: 817-822. (Pubitemid 46980491)
56. Paxinos G, Franklin KBJ (2001). The Mouse Brain in Stereotaxic Coordinates. Academic Press: San Diego.
57. Qiu HT, Meng HQ, Song C, Xiu MH, Chen da C, Zhu FY et al (2009). Association between monoamine oxidase (MAO)-A gene variants and schizophrenia in a Chinese population. Brain Res 1287: 67-73.
58. Ralph RJ, Paulus MP, Fumagalli F, Caron MG, Geyer MA (2001). Prepulse inhibition deficits and perseverative motor patterns in dopamine transporter knockout mice: differential effects of D1 and D2 receptor antagonists. J Neurosci 21: 305-313. (Pubitemid 32098754)
59. Risbrough VB, Masten VL, Caldwell S, Paulus MP, Low MJ, Geyer MA (2006). Differential contributions of dopamine D1, D2, and D3 receptors to MDMA-induced effects on loco-motor behavior patterns in mice. Neuropsychopharmacology 31: 2349-2358. (Pubitemid 44607051)
60. Rodgers RJ, Cole JC, Cobain MR, Daly P, Doran PJ, Eells JR et al (1992). Anxiogenic-like effects of fluprazine and eltoprazine in the mouse elevated plus-maze: profile comparisons with 8-OH-DPAT, CGS 12066B, TFMPP and mCPP. Behav Pharmacol 3: 621-634. (Pubitemid 23009881)
61. Salichon N, Gaspar P, Upton AL, Picaud S, Hanoun N, Hamon M et al (2001). Excessive activation of serotonin (5-HT) 1B receptors disrupts the formation of sensory maps in monoamine oxidase a and 5-ht transporter knockout mice. J Neurosci 21: 884-896. (Pubitemid 32163130)
62. Saxena S, Brody AL, Schwartz JM, Baxter LR (1998). Neuroimaging and frontal-subcortical circuitry in obsessive-compulsive disorder. Br J Psychiatry Suppl 35: 26-37. (Pubitemid 28368348)
63. Saxena S, Rauch SL (2000). Functional neuroimaging and the neuroanatomy of obsessive-compulsive disorder. Psychiatr Clin North Am 23: 563-586. (Pubitemid 30666507)
64. Schneider R, Hoffmann HJ, Schicknick H, Moutier R (1992). Genetic analysis of isolation-induced aggression. I. Comparison between closely related inbred mouse strains. Behav Neural Biol 57: 198-204.
65. Scott AL, Bortolato M, Chen K, Shih JC (2008). Novel monoamine oxidase A knockout mice with human-like spontaneous mutation. Neuroreport 19: 739-743. (Pubitemid 351555982)
66. Shih JC, Chen K, Ridd MJ (1999a). Monoamine oxidase: from genes to behavior. Annu Rev Neurosci 22: 197-217. (Pubitemid 29144886)
67. Shih JC, Thompson RF (1999b). Monoamine oxidase in neuro-psychiatry and behavior. Am J Hum Genet 65: 593-598.
68. Sholl DA (1956). The measurable parameters of the cerebral cortex and their significance in its organization. Prog Neurobiol 2: 324-333.
69. Simon P, Dupuis R, Costentin J (1994). Thigmotaxis as an index of anxiety in mice. Influence of dopaminergic transmissions. Behav Brain Res 61: 59-64. (Pubitemid 24097017)
70. Strolin Benedetti M, Boucher T, Fowler CJ (1983). The deamination of noradrenaline and 5-hydroxytryptamine by rat brain and heart monoamine oxidase and their inhibition by cimoxatone, toloxatone and MD 770222. Naunyn Schmiedebergs Arch Pharmacol 323: 315-320. (Pubitemid 13039069)
71. Szeszko PR, MacMillan S, McMeniman M, Lorch E, Madden R, Ivey J et al (2004). Amygdala volume reductions in pediatric patients with obsessive-compulsive disorder treated with paroxetine: preliminary findings. Neuropsychopharmacology 29: 826-832. (Pubitemid 38402491)
72. Szeszko PR, Robinson D, Alvir JM, Bilder RM, Lencz T, Ashtari M et al (1999). Orbital frontal and amygdala volume reductions in obsessive-compulsive disorder. Arch Gen Psychiatry 56: 913-919. (Pubitemid 29480127)
73. Tassone F, Qi L, Zhang W, Hansen RL, Pessah IN, Hertz-Picciotto I (2011). MAOA, DBH, and SLC6A4 variants in CHARGE: a case-control study of autism spectrum disorders. Autism Res (in press).
74. Teicher MH, Andersen SL, Polcari A, Anderson CM, Navalta CP, Kim DM (2003). The neurobiological consequences of early stress and childhood maltreatment. Neurosci Biobehav Rev 27: 33-44. (Pubitemid 36537818)
75. Treit D, Fundytus M (1988). Thigmotaxis as a test for anxiolytic activity in rats. Pharmacol Biochem Behav 31: 959-962. (Pubitemid 19274312)
76. Trullas R, Skolnick P (1993). Differences in fear motivated behaviors among inbred mouse strains. Psychopharmacology 111: 323-331. (Pubitemid 23165262)
77. Wellman CL, Izquierdo A, Garrett JE, Martin KP, Carroll J, Millstein R et al (2007). Impaired stress-coping and fear extinction and abnormal corticolimbic morphology in serotonin transporter knockout mice. J Neurosci 27: 684-691. (Pubitemid 46143772)
78. Williams LM, Gatt JM, Kuan SA, Dobson-Stone C, Palmer DM, Paul RH et al (2009). A polymorphism of the MAOA gene is associated with emotional brain markers and personality traits on an antisocial index. Neuropsychopharmacology 34: 1797-1809.
79. Williams RS, Ferrante RJ, Caviness Jr VS (1978). The Golgi rapid method in clinical neuropathology: the morphological consequences of suboptimal fixation. J Neuropathol Exp Neurol 37: 13-33. (Pubitemid 8266780)
80. Zald DH, Kim SW (1996a). Anatomy and function of the orbital frontal cortex, I: Anatomy, neurocircuitry; and obsessive-compulsive disorder. J Neuropsychiatry Clin Neurosci 8: 125-138. (Pubitemid 26138918)
81. Zald DH, Kim SW (1996b). Anatomy and function of the orbital frontal cortex, II: Function and relevance to obsessive-compulsive disorder. J Neuropsychiatry Clin Neurosci 8: 249-261. (Pubitemid 26275735)