Serotonin, genetic variability, behaviour, and psychiatric disorders - A review

Upsala Journal of Medical Sciences

Volumn 115, Issue 1, 2010, Pages 2-10

  Nordquist, Niklas ^a   Oreland, Lars ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

Behaviour; Development; Genetic polymorphism; Limbic system; MAOA; Psychiatric disorder; Serotonin; Sexual dichotomy; SLC6A4

Indexed keywords

AMINE OXIDASE (FLAVIN CONTAINING); NEUROLEPTIC AGENT; SEROTONIN; SEROTONIN TRANSPORTER;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; BRAIN; FEMALE; GENETIC VARIABILITY; GENETICS; HUMAN; MALE; MENTAL DISEASE; METABOLISM; PRENATAL DEVELOPMENT; RISK FACTOR;

ANIMALS; ANTIPSYCHOTIC AGENTS; BRAIN; FEMALE; GENETIC VARIATION; HUMANS; MALE; MENTAL DISORDERS; MODELS, BIOLOGICAL; MONOAMINE OXIDASE; RISK FACTORS; SEROTONIN; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS;

EID: 77749330369     PISSN: 03009734     EISSN: None     Source Type: Journal    
DOI: 10.3109/03009730903573246     Document Type: Article

References (87)

1. Little KY, McLaughlin DP, Zhang L, Livermore CS, Dalack GW, McFinton PR, et al. Cocaine, ethanol, and genotype effects on human midbrain serotonin transporter binding sites and mRNA levels. Am J Psychiatry. 1998; 155:207-213
2. Sabol SZ, Hu S, Hamer D. A functional polymorphism in the monoamine oxidase A gene promoter. Hum Genet. 1998; 103:273-279
3. Deckert J, Catalano M, Syagailo YV, Bosi M, Okladnova O, Di Bella D, et al. Excess of high activity monoamine oxidase A gene promoter alleles in female patients with panic disorder. Hum Mol Genet. 1999;8:621-624
4. Denney RM, Koch H, Craig IW. Association between monoamine oxidase A activity in human male skin fibroblasts and genotype of the MAOA promoter-associated variable number tandem repeat. Hum Genet. 1999;105: 542-551
5. Bennett AJ, Lesch KP, Heils A, Long JC, Lorenz JG, Shoaf SE, et al. Early experience and serotonin transporter gene variation interact to influence primate CNS function. Mol Psychiatry. 2002;7:118-122
6. Newman TK, Syagailo YV, Barr CS, Wendland JR, Champoux M, Graessle M, et al. Monoamine oxidase A gene promoter variation and rearing experience influences aggressive behavior in rhesus monkeys. Biol Psychiatry. 2005;57:167-172
7. Hu XZ, Lipsky RH, Zhu G, Akhtar LA, Taubman J, Greenberg BD, et al. Serotonin transporter promoter gainof-function genotypes are linked to obsessive-compulsive disorder. Am J Hum Genet. 2006;78:815-826
8. Guo G, Ou XM, Roettger M, Shih JC. The VNTR 2 repeat in MAOA and delinquent behavior in adolescence and young adulthood: associations and MAOA promoter activity. Eur J Hum Genet. 2008;16:626-634
9. Lesch KP, Bengel D, Heils A, Sabol SZ, Greenberg BD, Petri S, et al. Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science. 1996;274:1527-1531
10. Caspi A, McClay J, Moffitt TE, Mill J, Martin J, Craig IW, et al. Role of genotype in the cycle of violence in maltreated children. Science. 2002;297:851-854
11. Caspi A, Sugden K, Moffitt TE, Taylor A, Craig IW, Harrington H, et al. Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science. 2003;301:386-389
12. Nilsson KW, Sjoberg RL, Damberg M, Leppert J, Ohrvik J, Alm PO, et al. Role of monoamine oxidase A genotype and psychosocial factors in male adolescent criminal activity. Biol Psychiatry. 2006;59:121-127
13. Sjoberg RL, Nilsson KW, Nordquist N, Ohrvik J, Leppert J, Lindstrom L, et al. Development of depression: sex and the interaction between environment and a promoter polymorphism of the serotonin transporter gene. Int J Neuropsychopharmacol. 2006;9:443-449
14. Nilsson KW, Wargelius HL, Sjoberg RL, Leppert J, Oreland L. The MAO-A gene, platelet MAO-B activity and psychosocial environment in adolescent female alcoholrelated problem behaviour. Drug Alcohol Depend. 2008; 93:51-62.
15. Lau JY, Goldman D, Buzas B, Fromm SJ, Guyer AE, Hodgkinson C, et al. Amygdala function and 5-HTT gene variants in adolescent anxiety and major depressive disorder. Biol Psychiatry. 2009;65:349-355
16. Nakamura M, Ueno S, Sano A, Tanabe H. The human serotonin transporter gene linked polymorphism (5-HTTLPR) shows ten novel allelic variants. Mol Psychiatry. 2000;5:32-38
17. Kraft JB, Slager SL, McGrath PJ, Hamilton SP. Sequence analysis of the serotonin transporter and associations with antidepressant response. Biol Psychiatry. 2005;58:374-381
18. Lesch KP, Meyer J, Glatz K, Flugge G, Hinney A, Hebebrand J, et al. The 5-HT transporter gene-linked polymorphic region (5-HTTLPR) in evolutionary perspective: alternative biallelic variation in rhesus monkeys. Rapid communication. J Neural Transm. 1997;104:1259-1266
19. Willeit M, Stastny J, Pirker W, Praschak-Rieder N, Neumeister A, Asenbaum S, et al. No evidence for in vivo regulation of midbrain serotonin transporter availability by serotonin transporter promoter gene polymorphism. Biol Psychiatry. 2001;50:8-12.
20. Shioe K, Ichimiya T, Suhara T, Takano A, Sudo Y, Yasuno F, et al. No association between genotype of the promoter region of serotonin transporter gene and serotonin transporter binding in human brain measured by PET. Synapse. 2003; 48:184-188
21. Parsey RV, Hastings RS, Oquendo MA, Hu X, Goldman D, Huang YY, et al. Effect of a triallelic functional polymorphism of the serotonin-transporter- linked promoter region on expression of serotonin transporter in the human brain. Am J Psychiatry. 2006;163:48-51.
22. Christian BT, Fox AS, Oler JA, Vandehey NT, Murali D, Rogers J, et al. Serotonin transporter binding and genotype in the nonhuman primate brain using [C-11]DASB PET. NeuroImage. 2009;47:1230-1236
23. Jedema HP, Gianaros PJ, Greer PJ, Kerr DD, Liu S, Higley JD, et al. Cognitive impact of genetic variation of the serotonin transporter in primates is associated with differences in brain morphology rather than serotonin neurotransmission. MolPsychiatry. 2009 Sep 1 (Epub ahead of print)
24. Fowler JS, Alia-Klein N, Kriplani A, Logan J, Williams B, Zhu W, et al. Evidence that brain MAO A activity does not correspond to MAO A genotype in healthy male subjects. Biol Psychiatry. 2007;62:355-358
25. Alia-Klein N, Goldstein RZ, Kriplani A, Logan J, Tomasi D, Williams B, et al. Brain monoamine oxidase A activity predicts trait aggression. J Neurosci. 2008;28:5099-5104
26. Alia-Klein N, Kriplani A, Pradhan K, Ma JY, Logan J, Williams B, et al. The MAO-A genotype does not modulate resting brain metabolism in adults. Psychiatry Res. 2008; 164:73-76
27. Balciuniene J, Emilsson L, Oreland L, Pettersson U, Jazin E. Investigation of the functional effect of monoamine oxidase polymorphisms in human brain. Hum Genet. 2002; 110:1-7.
28. Cirulli ET, Goldstein DB. In vitro assays fail to predict in vivo effects of regulatory polymorphisms. Hum Mol Genet. 2007;16:1931-1939
29. Soubrié P. Reconciling the role of central serotonin neurons in human and animal behavior. Behav Brain Sci. 1986;9:319-364
30. Sundstrom E, Kolare S, Souverbie F, Samuelsson EB, Pschera H, Lunell NO, et al. Neurochemical differentiation of human bulbospinal monoaminergic neurons during the first trimester. Brain Res Dev Brain Res. 1993;75:1-12.
31. Moiseiwitsch JR, Lauder JM. Serotonin regulates mouse cranial neural crest migration. Proc Natl Acad Sci U S A. 1995;92:7182-7186
32. Gustafsson BI, Tommeras K, Nordrum I, Loennechen JP, Brunsvik A, Solligard E, et al. Long-term serotonin administration induces heart valve disease in rats. Circulation. 2005;111:1517-1522
33. Brunner HG, Nelen M, Breakefield XO, Ropers HH, van Oost BA. Abnormal behavior associated with a point mutation in the structural gene for monoamine oxidase A. Science. 1993;262:578-580
34. Cases O, Seif I, Grimsby J, Gaspar P, Chen K, Pournin S, et al. Aggressive behavior and altered amounts of brain serotonin and norepinephrine in mice lacking MAOA. Science. 1995;268:1763-1766
35. Popova NK, Maslova LN, Morosova EA, Bulygina VV, Seif I. MAOA knockout attenuates adrenocortical response to various kinds of stress. Psychoneuroendocrinology. 2006;31:179-186
36. Scott AL, Bortolato M, Chen K, Shih JC. Novel monoamine oxidase A knock out mice with human-like spontaneous mutation. Neuroreport. 2008;19:739-743
37. Holmes A, Lit Q, Murphy DL, Gold E, Crawley JN. Abnormal anxiety-related behavior in serotonin transporter null mutant mice: the influence of genetic background. Genes Brain Behav. 2003;2:365-380
38. Kalueff AV, Olivier JD, Nonkes LJ, Homberg JR. Conserved role for the serotonin transporter gene in rat and mouse neurobehavioral endophenotypes. Neurosci Biobehav Rev. 2009 Aug 19 (Epub ahead of print).
39. Noorlander CW, Ververs FF, Nikkels PG, van Echteld CJ, Visser GH, Smidt MP. Modulation of serotonin transporter function during fetal development causes dilated heart cardiomyopathy and lifelong behavioral abnormalities. PloS One. 2008;3:e2782.
40. Ansorge MS, Morelli E, Gingrich JA. Inhibition of serotonin but not norepinephrine transport during development produces delayed, persistent perturbations of emotional behaviors in mice. J Neurosci. 2008;28:199-207.
41. Clancy B, Kersh B, Hyde J, Darlington RB, Anand KJ, Finlay BL. Web-based method for translating neurodevelopment from laboratory species to humans. Neuroinformatics. 2007;5:79-94.
42. Mejia JM, Ervin FR, Baker GB, Palmour RM. Monoamine oxidase inhibition during brain development induces pathological aggressive behavior in mice. Biol Psychiatry. 2002; 52:811-821
43. Hendricks T, Francis N, Fyodorov D, Deneris ES. The ETS domain factor Pet-1 is an early and precise marker of central serotonin neurons and interacts with a conserved element in serotonergic genes. J Neurosci. 1999;19:10348-10356
44. Hendricks TJ, Fyodorov DV, Wegman LJ, Lelutiu NB, Pehek EA, Yamamoto B, et al. Pet-1 ETS gene plays a critical role in 5-HT neuron development and is required for normal anxiety-like and aggressive behavior. Neuron. 2003;37:233-247
45. Beaulieu JM, Zhang X, Rodriguiz RM, Sotnikova TD, Cools MJ, Wetsel WC, et al. Role of GSK3 beta in behavioral abnormalities induced by serotonin deficiency. Proc Natl Acad Sci U S A. 2008;105:1333-1338
46. Alenina N, Kikic D, Todiras M, Mosienko V, Qadri F, Plehm R, et al. Growth retardation and altered autonomic control in mice lacking brain serotonin. Proc Natl Acad Sci U S A. 2009;106:10332-10337
47. Killackey HP, Rhoades RW, Bennett-Clarke CA. The formation of a cortical somatotopic map. Trends Neurosci. 1995; 18:402-407
48. Cases O, Vitalis T, Seif I, De Maeyer E, Sotelo C, Gaspar P. Lack of barrels in the somatosensory cortex of monoamine oxidase A-deficient mice: role of a serotonin excess during the critical period. Neuron. 1996;16:297-307.
49. Vitalis T, Cases O, Callebert J, Launay JM, Price DJ, Seif I, et al. Effects of monoamine oxidase A inhibition on barrel formation in the mouse somatosensory cortex: determination of a sensitive developmental period. J Comp Neurol. 1998; 393:169-184
50. Persico AM, Mengual E, Moessner R, Hall FS, Revay RS, Sora I, et al. Barrel pattern formation requires serotonin uptake by thalamocortical afferents, and not vesicular monoamine release. J Neurosci. 2001;21:6862-6873
51. Xu Y, Sari Y, Zhou FC. Selective serotonin reuptake inhibitor disrupts organization of thalamocortical somatosensory barrels during development. Brain Res Dev Brain Res. 2004; 150:151-161
52. Auso E, Cases O, Fouquet C, CamachoM, Garcia-Velasco JV, Gaspar P, et al. Protracted expression of serotonin transporter and altered thalamocortical projections in the barrelfield of hypothyroid rats. Eur J Neurosci. 2001;14:1968-1980
53. Salichon N, Gaspar P, Upton AL, Picaud S, Hanoun N, Hamon M, et al. Excessive activation of serotonin (5-HT) 1B receptors disrupts the formation of sensory maps in monoamine oxidase a and 5-ht transporter knock-out mice. J Neurosci. 2001;21:884-896
54. Rebsam A, Seif I, Gaspar P. Refinement of thalamocortical arbors and emergence of barrel domains in the primary somatosensory cortex: a study of normal and monoamine oxidase a knock-out mice. J Neurosci. 2002;22:8541-8552
55. Laurent A, Goaillard JM, Cases O, Lebrand C, Gaspar P, Ropert N. Activity-dependent presynaptic effect of serotonin 1B receptors on the somatosensory thalamocortical transmission in neonatal mice. J Neurosci. 2002;22:886-900.
56. Hariri AR, Mattay VS, Tessitore A, Kolachana B, Fera F, Goldman D, et al. Serotonin transporter genetic variation and the response of the human amygdala. Science. 2002; 297:400-403
57. Hariri AR, Drabant EM, Munoz KE, Kolachana BS, Mattay VS, Egan MF, et al. A susceptibility gene for affective disorders and the response of the human amygdala. Arch Gen Psychiatry. 2005;62:146-152
58. Pezawas L,Meyer-Lindenberg A,DrabantEM, Verchinski BA, Munoz KE, Kolachana BS, et al. 5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: a genetic susceptibility mechanism for depression. Nat Neurosci. 2005; 8:828-834
59. Meyer-Lindenberg A, Buckholtz JW, Kolachana B, R Hariri A, Pezawas L, Blasi G, et al. Neural mechanisms of genetic risk for impulsivity and violence in humans. Proc Natl Acad Sci U S A. 2006;103:6269-6274
60. Buckholtz JW, Callicott JH, Kolachana B, Hariri AR, Goldberg TE, Genderson M, et al. Genetic variation in MAOA modulates ventromedial prefrontal circuitry mediating individual differences in human personality. Mol Psychiatry. 2008;13:313-324
61. Passamonti L, Cerasa A, Gioia MC,Magariello A, Muglia M, Quattrone A, et al. Genetically dependent modulation of serotonergic inactivation in the human prefrontal cortex. NeuroImage. 2008;40:1264-1273
62. Pacheco J, Beevers CG, Benavides C, McGeary J, Stice E, Schnyer DM. Frontal-limbic white matter pathway associations with the serotonin transporter gene promoter region (5-HTTLPR) polymorphism. J Neurosci. 2009;29:6229-6233
63. Paton JJ, Belova MA, Morrison SE, Salzman CD. The primate amygdala represents the positive and negative value of visual stimuli during learning. Nature. 2006;439:865-870
64. Wellman CL, Izquierdo A, Garrett JE, Martin KP, Carroll J, Millstein R, et al. Impaired stress-coping and fear extinction and abnormal corticolimbic morphology in serotonin transporter knock-out mice. J Neurosci. 2007;27:684-691
65. Bearer EL, Zhang X, Janvelyan D, Boulat B, Jacobs RE. Reward circuitry is perturbed in the absence of the serotonin transporter. NeuroImage. 2009;46:1091-1104
66. Narboux-Neme N, Pavone LM, Avallone L, Zhuang X, Gaspar P. Serotonin transporter transgenic (SERTcre) mouse line reveals developmental targets of serotonin specific reuptake inhibitors (SSRIs). Neuropharmacology. 2008; 55:994-1005.
67. Whitaker-Azmitia PM. Behavioral and cellular consequences of increasing serotonergic activity during brain development: a role in autism? Int J Dev Neurosci. 2005;23:75-83.
68. Young SN, Leyton M. The role of serotonin in human mood and social interaction. Insight from altered tryptophan levels. Pharmacol Biochem Behav. 2002;71:857-865
69. Fusar-Poli P, Allen P, McGuire P, Placentino A, Cortesi M, Perez J. Neuroimaging and electrophysiological studies of the effects of acute tryptophan depletion: a systematic review of the literature. Psychopharmacology. 2006;188:131-143
70. Firk C, Markus CR. Differential effects of 5-HTTLPR genotypes on mood, memory, and attention bias following acute tryptophan depletion and stress exposure. Psychopharmacology. 2009;203:805-818
71. Munafo MR, Brown SM, Hariri AR. Serotonin transporter (5-HTTLPR) genotype and amygdala activation: a metaanalysis. Biol Psychiatry. 2008;63:852-857
72. Walderhaug E, Magnusson A, Neumeister A, Lappalainen J, Lunde H, Refsum H, et al. Interactive effects of sex and 5-HTTLPR on mood and impulsivity during tryptophan depletion in healthy people. Biol Psychiatry. 2007;62: 593-599
73. Brummett BH, Muller CL, Collins AL, Boyle SH, Kuhn CM, Siegler IC, et al. 5-HTTLPR and gender moderate changes in negative affect responses to tryptophan infusion. Behav Genet. 2008;38:476-483
74. Markus CR, Firk C. Differential effects of tri-allelic 5-HTTLPR polymorphisms in healthy subjects on mood and stress performance after tryptophan challenge. Neuropsychopharmacology. 2009;34:2667-2674
75. Sjoberg RL, Nilsson KW, Wargelius HL, Leppert J, Lindstrom L, Oreland L. Adolescent girls and criminal activity: role of MAOA-LPR genotype and psychosocial factors. Am J Med Genet B Neuropsychiatr Genet. 2007;144B: 159-164
76. Nilsson KW, Sjoberg RL, Wargelius HL, Leppert J, Lindstrom L, Oreland L. The monoamine oxidase A (MAO-A) gene, family function and maltreatment as predictors of destructive behaviour during male adolescent alcohol consumption. Addiction. 2007;102:389-398
77. Barr CS, Newman TK, Schwandt M, Shannon C, Dvoskin RL, Lindell SG, et al. Sexual dichotomy of an interaction between early adversity and the serotonin transporter gene promoter variant in rhesus macaques. Proc Natl Acad Sci U S A. 2004;101:12358-12363
78. Arnold AP. Sex chromosomes and brain gender. Nat Rev Neurosci. 2004;5:701-708
79. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR, et al. Epigenetic programming by maternal behavior. Nat Neurosci. 2004;7:847-854
80. Holden C. Sex and the suffering brain. Science. 2005; 308:1574.
81. Cahill L. Why sex matters for neuroscience. Nat Rev Neurosci. 2006;7:477-484
82. Spinelli S, Chefer S, Suomi SJ, Higley JD, Barr CS, Stein E. Early-life stress induces long-term morphologic changes in primate brain. Arch Gen Psychiatry. 2009;66:658-665
83. Cirulli F, Francia N, Branchi I, Antonucci MT, Aloe L, Suomi SJ, et al. Changes in plasma levels of BDNF and NGF reveal a gender-selective vulnerability to early adversity in rhesus macaques. Psychoneuroendocrinology. 2009;34: 172-180
84. Ren-Patterson RF, Cochran LW, Holmes A, Sherrill S, Huang SJ, Tolliver T, et al. Loss of brain-derived neurotrophic factor gene allele exacerbates brain monoamine deficiencies and increases stress abnormalities of serotonin transporter knockout mice. J Neurosci Res. 2005;79: 756-771
85. Pezawas L, Meyer-Lindenberg A, Goldman AL, Verchinski BA, Chen G, Kolachana BS, et al. Evidence of biologic epistasis between BDNF and SLC6A4 and implications for depression. Mol Psychiatry. 2008;13:709-716
86. Oreland S, Pickering C, Gokturk C, Oreland L, Arborelius L, Nylander I. Two repeated maternal separation procedures differentially affect brain 5-hydroxytryptamine transporter and receptors in young and adult male and female rats. Brain Res. 2009;1305 Suppl:S37-49.
87. Kuramochi M, Nakamura S. Effects of postnatal isolation rearing and antidepressant treatment on the density of serotonergic and noradrenergic axons and depressive behavior in rats. Neuroscience. 2009;163:448-455