Early-life serotonin dysregulation affects the migration and positioning of cortical interneuron subtypes

Translational Psychiatry

Volumn 5, Issue 9, 2015, Pages

  Frazer, S ^a   Otomo, K ^a   Dayer, A ^a  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; FLUOXETINE; GASTROINTESTINAL POLYPEPTIDE; GLUTAMATE DECARBOXYLASE 65; NEUROPEPTIDE Y; PARVALBUMIN; REELIN; SEROTONIN; SEROTONIN RECEPTOR; SEROTONIN TRANSPORTER; SOMATOSTATIN; SEROTONIN UPTAKE INHIBITOR; SLC6A4 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL MIGRATION; CONTROLLED STUDY; INTERNEURON; MEDIAN EMINENCE; MENTAL DISEASE; MOUSE; NERVE CELL GROWTH; NEWBORN; NONHUMAN; PERINATAL PERIOD; PROTEIN EXPRESSION; SOMATOSENSORY CORTEX; SUBVENTRICULAR ZONE; TIME LAPSE IMAGING; TRANSCRIPTION REGULATION; ANIMAL; BRAIN CORTEX; CELL MEMBRANE; DISEASE MODEL; DRUG EFFECTS; EMBRYOLOGY; FEMALE; GENE EXPRESSION REGULATION; METABOLISM; PREGNANCY; PRENATAL EXPOSURE;

ANIMALS; CELL MEMBRANE; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; FEMALE; FLUOXETINE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INTERNEURONS; MENTAL DISORDERS; MICE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SEROTONIN; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; SEROTONIN UPTAKE INHIBITORS;

EID: 84977765160     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2015.147     Document Type: Article

References (89)

1. Huang ZJ. Toward a genetic dissection of cortical circuits in the mouse. Neuron 2014; 83: 1284-1302.
2. Marin O, Valiente M, Ge X, Tsai LH. Guiding neuronal cell migrations. Cold Spring Harb Protoc 2010; 2: a001834.
3. Valiente M, Marin O. Neuronal migration mechanisms in development and disease. Curr Opin Neurobiol 2010; 20: 68-78.
4. Todtenkopf MS, Vincent SL, Benes FM. A cross-study meta-analysis and threedimensional comparison of cell counting in the anterior cingulate cortex of schizophrenic and bipolar brain. Schizophr Res 2005; 73: 79-89.
5. Lewis DA, Hashimoto T, Volk DW. Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 2005; 6: 312-324.
6. Marin O. Interneuron dysfunction in psychiatric disorders. Nat Rev Neurosci 2012; 13: 107-120.
7. Gaspar P, Cases O, Maroteaux L. The developmental role of serotonin: news from mouse molecular genetics. Nat Rev Neurosci 2003; 4: 1002-1012.
8. Vitalis T, Ansorge MS, Dayer AG. Serotonin homeostasis and serotonin receptors as actors of cortical construction: special attention to the 5-HT3A and 5-HT6 receptor subtypes. Front Cell Neurosci 2013; 7: 93.
9. Dayer A. Serotonin-related pathways and developmental plasticity: relevance for psychiatric disorders. Dialogues Clin Neurosci 2014; 16: 29-41.
10. Bonnin A, Goeden N, Chen K, Wilson ML, King J, Shih JC et al. A transient placental source of serotonin for the fetal forebrain. Nature 2011; 472: 347-350.
11. Homberg JR, Schubert D, Gaspar P. New perspectives on the neurodevelopmental effects of SSRIs. Trends Pharmacol Sci 2010; 31: 60-65.
12. 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; 34: 373-386.
13. Oberlander TF, Gingrich JA, Ansorge MS. Sustained neurobehavioral effects of exposure to SSRI antidepressants during development: molecular to clinical evidence. Clin Pharmacol Ther 2009; 86: 672-677.
14. Murphy DL, Lesch KP. Targeting the murine serotonin transporter: insights into human neurobiology. Nat Rev Neurosci 2008; 9: 85-96.
15. Karg K, Burmeister M, Shedden K, Sen S. The serotonin transporter promoter variant (5-HTTLPR), stress, and depression meta-analysis revisited: evidence of genetic moderation. Arch Gen Psychiatry 2011; 68: 444-454.
16. 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.
17. Pluess M, Velders FP, Belsky J, van IJMH, Bakermans-Kranenburg MJ, Jaddoe VW et al. Serotonin transporter polymorphism moderates effects of prenatal maternal anxiety on infant negative emotionality. Biol Psychiatry 2011; 69: 520-525.
18. Champoux M, Bennett A, Shannon C, Higley JD, Lesch KP, Suomi SJ. Serotonin transporter gene polymorphism, differential early rearing, and behavior in rhesus monkey neonates. Mol Psychiatry 2002; 7: 1058-1063.
19. Pezawas L, Meyer-Lindenberg A, Drabant EM, 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.
20. Munafo MR, Brown SM, Hariri AR. Serotonin transporter (5-HTTLPR) genotype and amygdala activation: a meta-analysis. Biol Psychiatry 2008; 63: 852-857.
21. Clements CC, Castro VM, Blumenthal SR, Rosenfield HR, Murphy SN, Fava M et al. Prenatal antidepressant exposure is associated with risk for attention-deficit hyperactivity disorder but not autism spectrum disorder in a large health system. Mol Psychiatry 2014; 20: 727-734.
22. Rai D, Lee BK, Dalman C, Golding J, Lewis G, Magnusson C. Parental depression, maternal antidepressant use during pregnancy, and risk of autism spectrum disorders: population based case-control study. Br Med J 2013; 346: f2059.
23. Croen LA, Grether JK, Yoshida CK, Odouli R, Hendrick V. Antidepressant use during pregnancy and childhood autism spectrum disorders. Arch Gen Psychiatry 2011; 68: 1104-1112.
24. Vucurovic K, Gallopin T, Ferezou I, Rancillac A, Chameau P, van Hooft JA et al. Serotonin 3A receptor subtype as an early and protracted marker of cortical interneuron subpopulations. Cereb Cortex 2010; 20: 2333-2347.
25. Lee S, Hjerling-Leffler J, Zagha E, Fishell G, Rudy B. The largest group of superficial neocortical GABAergic interneurons expresses ionotropic serotonin receptors. J Neurosci 2010; 30: 16796-16808.
26. Murthy S, Niquille M, Hurni N, Limoni G, Frazer S, Chameau P et al. Serotonin receptor 3A controls interneuron migration into the neocortex. Nat Commun 2014; 5: 5524.
27. Riccio O, Murthy S, Szabo G, Vutskits L, Kiss JZ, Vitalis T et al. New pool of cortical interneuron precursors in the early postnatal dorsal white matter. Cereb Cortex 2012; 22: 86-98.
28. Lira A, Zhou M, Castanon N, Ansorge MS, Gordon JA, Francis JH et al. Altered depression-related behaviors and functional changes in the dorsal raphe nucleus of serotonin transporter-deficient mice. Biol Psychiatry 2003; 54: 960-971.
29. Covington HEr, Maze I, LaPlant QC, Vialou VF, Ohnishi YN, Berton O et al. Antidepressant actions of histone deacetylase inhibitors. J Neurosci 2009; 29: 11451-11460.
30. Riccio O, Jacobshagen M, Golding B, Vutskits L, Jabaudon D, Hornung JP et al. Excess of serotonin affects neocortical pyramidal neuron migration. Transl Psychiatry 2011; 1: e47.
31. Riccio O, Potter G, Walzer C, Vallet P, Szabo G, Vutskits L et al. Excess of serotonin affects embryonic interneuron migration through activation of the serotonin receptor 6. Mol Psychiatry 2009; 14: 280-290.
32. Shintani T, Takeuchi Y, Fujikawa A, Noda M. Directional neuronal migration is impaired in mice lacking adenomatous polyposis coli 2. J Neurosci 2012; 32: 6468-6484.
33. Eom TY, Stanco A, Guo J, Wilkins G, Deslauriers D, Yan J et al. Differential regulation of microtubule severing by APC underlies distinct patterns of projection neuron and interneuron migration. Dev Cell 2014; 31: 677-689.
34. Marin O, Plump AS, Flames N, Sanchez-Camacho C, Tessier-Lavigne M, Rubenstein JL. Directional guidance of interneuron migration to the cerebral cortex relies on subcortical Slit1/2-independent repulsion and cortical attraction. Development 2003; 130: 1889-1901.
35. Wu W, Wong K, Chen J, Jiang Z, Dupuis S, Wu JY et al. Directional guidance of neuronal migration in the olfactory system by the protein Slit. Nature 1999; 400: 331-336.
36. Cariboni A, Andrews WD, Memi F, Ypsilanti AR, Zelina P, Chedotal A et al. Slit2 and Robo3 modulate the migration of GnRH-secreting neurons. Development 2012; 139: 3326-3331.
37. Zhang X, Lei K, Yuan X, Wu X, Zhuang Y, Xu T et al. SUN1/2 and Syne/Nesprin-1/2 complexes connect centrosome to the nucleus during neurogenesis and neuronal migration in mice. Neuron 2009; 64: 173-187.
38. Qu Y, Glasco DM, Zhou L, Sawant A, Ravni A, Fritzsch B et al. Atypical cadherins Celsr1-3 differentially regulate migration of facial branchiomotor neurons in mice. J Neurosci 2010; 30: 9392-9401.
39. Vivancos V, Chen P, Spassky N, Qian D, Dabdoub A, Kelley M et al. Wnt activity guides facial branchiomotor neuron migration, and involves the PCP pathway and JNK and ROCK kinases. Neural Dev 2009; 4: 7.
40. Paul V, Tonchev AB, Henningfeld KA, Pavlakis E, Rust B, Pieler T et al. Scratch2 modulates neurogenesis and cell migration through antagonism of bHLH proteins in the developing neocortex. Cereb Cortex 2014; 24: 754-772.
41. Watanabe K, Takebayashi H, Bepari AK, Esumi S, Yanagawa Y, Tamamaki N. Dpy19l1, a multi-transmembrane protein, regulates the radial migration of glutamatergic neurons in the developing cerebral cortex. Development 2011; 138: 4979-4990.
42. Toriyama M, Mizuno N, Fukami T, Iguchi T, Toriyama M, Tago K et al. Phosphorylation of doublecortin by protein kinase A orchestrates microtubule and actin dynamics to promote neuronal progenitor cell migration. J Biol Chem 2012; 287: 12691-12702.
43. Jaarsma D, van den Berg R, Wulf PS, van Erp S, Keijzer N, Schlager MA et al. A role for Bicaudal-D2 in radial cerebellar granule cell migration. Nat Commun 2014; 5: 3411.
44. Golding B, Pouchelon G, Bellone C, Murthy S, Di Nardo AA, Govindan S et al. Retinal input directs the recruitment of inhibitory interneurons into thalamic visual circuits. Neuron 2014; 81: 1057-1069.
45. Wortham M, Jin G, Sun JL, Bigner DD, He Y, Yan H. Aberrant Otx2 expression enhances migration and induces ectopic proliferation of hindbrain neuronal progenitor cells. PLoS One 2012; 7: e36211.
46. Clovis YM, Enard W, Marinaro F, Huttner WB, De Pietri Tonelli D. Convergent repression of Foxp2 3'UTR by miR-9 and miR-132 in embryonic mouse neocortex: implications for radial migration of neurons. Development 2012; 139: 3332-3342.
47. Godin JD, Thomas N, Laguesse S, Malinouskaya L, Close P, Malaise O et al. p27 (Kip1) is a microtubule-associated protein that promotes microtubule polymerization during neuron migration. Dev Cell 2012; 23: 729-744.
48. Nishimura YV, Shikanai M, Hoshino M, Ohshima T, Nabeshima Y, Mizutani K et al. Cdk5 and its substrates, Dcx and p27kip1, regulate cytoplasmic dilation formation and nuclear elongation in migrating neurons. Development 2014; 141: 3540-3550.
49. Stanco A, Szekeres C, Patel N, Rao S, Campbell K, Kreidberg JA et al. Netrin-1- alpha3beta1 integrin interactions regulate the migration of interneurons through the cortical marginal zone. Proc Natl Acad Sci USA 2009; 106: 7595-7600.
50. Fishell G, Rudy B. Mechanisms of Inhibition within the Telencephalon: "Where the Wild Things Are". Annu Rev Neurosci 2011; 34: 535-567.
51. Flames N, Pla R, Gelman DM, Rubenstein JL, Puelles L, Marin O. Delineation of multiple subpallial progenitor domains by the combinatorial expression of transcriptional codes. J Neurosci 2007; 27: 9682-9695.
52. Marin O. Cellular and molecular mechanisms controlling the migration of neocortical interneurons. Eur J Neurosci 2013; 38: 2019-2029.
53. Gelman DM, Marin O. Generation of interneuron diversity in the mouse cerebral cortex. Eur J Neurosci 2010; 31: 2136-2141.
54. Miyoshi G, Hjerling-Leffler J, Karayannis T, Sousa VH, Butt SJ, Battiste J et al. Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J Neurosci 2010; 30: 1582-1594.
55. Gelman DM, Martini FJ, Nobrega-Pereira S, Pierani A, Kessaris N, Marin O. The embryonic preoptic area is a novel source of cortical GABAergic interneurons. J Neurosci 2009; 29: 9380-9389.
56. Gelman D, Griveau A, Dehorter N, Teissier A, Varela C, Pla R et al. A wide diversity of cortical GABAergic interneurons derives from the embryonic preoptic area. J Neurosci 2011; 31: 16570-16580.
57. Mathews TA, Fedele DE, Coppelli FM, Avila AM, Murphy DL, Andrews AM. Gene dose-dependent alterations in extraneuronal serotonin but not dopamine in mice with reduced serotonin transporter expression. J Neurosci Methods 2004; 140: 169-181.
58. Koch S, Perry KW, Nelson DL, Conway RG, Threlkeld PG, Bymaster FP. R-fluoxetine increases extracellular DA, NE, as well as 5-HT in rat prefrontal cortex and hypothalamus: an in vivo microdialysis and receptor binding study. Neuropsychopharmacology 2002; 27: 949-959.
59. Miraoui H, Dwyer AA, Sykiotis GP, Plummer L, Chung W, Feng B et al. Mutations in FGF17, IL17RD, DUSP6, SPRY4, and FLRT3 are identified in individuals with congenital hypogonadotropic hypogonadism. Am J Hum Genet 2013; 92: 725-743.
60. Valdes-Socin H, Rubio Almanza M, Tome Fernandez-Ladreda M, Debray FG, Bours V, Beckers A. Reproduction, smell, and neurodevelopmental disorders: genetic defects in different hypogonadotropic hypogonadal syndromes. Front Endocrinol (Lausanne) 2014; 5: 109.
61. Mathews ES, Mawdsley DJ, Walker M, Hines JH, Pozzoli M, Appel B. Mutation of 3- hydroxy-3-methylglutaryl CoA synthase I reveals requirements for isoprenoid and cholesterol synthesis in oligodendrocyte migration arrest, axon wrapping, and myelin gene expression. J Neurosci 2014; 34: 3402-3412.
62. Jin FZ, Yu C, Zhao DZ, Wu MJ, Yang Z. A correlation between altered O-GlcNAcylation, migration and with changes in E-cadherin levels in ovarian cancer cells. Exp Cell Res 2013; 319: 1482-1490.
63. Ott LE, Sung EJ, Melvin AT, Sheats MK, Haugh JM, Adler KB et al. Fibroblast migration is regulated by myristoylated alanine-rich C-kinase substrate (MARCKS) protein. PLoS One 2013; 8: e66512.
64. Sheats MK, Sung EJ, Adler KB, Jones SL. In vitro neutrophil migration requires protein kinase C-Delta (delta-PKC)-mediated myristoylated alanine-rich C-kinase substrate (MARCKS) phosphorylation. Inflammation 2014; 38: 1126-1141.
65. Kalwa H, Michel T. The MARCKS protein plays a critical role in phosphatidylinositol 4,5-bisphosphate metabolism and directed cell movement in vascular endothelial cells. J Biol Chem 2011; 286: 2320-2330.
66. Lee S, Jang E, Kim JH, Kim JH, Lee WH, Suk K. Lipocalin-type prostaglandin D2 synthase protein regulates glial cell migration and morphology through myristoylated alanine-rich C-kinase substrate: prostaglandin D2-independent effects. J Biol Chem 2012; 287: 9414-9428.
67. Ericson E, Gebbia M, Heisler LE, Wildenhain J, Tyers M, Giaever G et al. Off-target effects of psychoactive drugs revealed by genome-wide assays in yeast. PLoS Genet 2008; 4: e1000151.
68. Ni YG, Miledi R. Blockage of 5HT2C serotonin receptors by fluoxetine (Prozac). Proc Natl Acad Sci USA 1997; 94: 2036-2040.
69. Garcia-Colunga J, Awad JN, Miledi R. Blockage of muscle and neuronal nicotinic acetylcholine receptors by fluoxetine (Prozac). Proc Natl Acad Sci USA 1997; 94: 2041-2044.
70. Kobayashi T, Washiyama K, Ikeda K. Inhibition of G protein-activated inwardly rectifying K+ channels by fluoxetine (Prozac). Br J Pharmacol 2003; 138: 1119-1128.
71. Kennard LE, Chumbley JR, Ranatunga KM, Armstrong SJ, Veale EL, Mathie A. Inhibition of the human two-pore domain potassium channel, TREK-1, by fluoxetine and its metabolite norfluoxetine. Br J Pharmacol 2005; 144: 821-829.
72. Heurteaux C, Lucas G, Guy N, El Yacoubi M, Thummler S, Peng XD et al. Deletion of the background potassium channel TREK-1 results in a depression-resistant phenotype. Nat Neurosci 2006; 9: 1134-1141.
73. Dong YY, Pike AC, Mackenzie A, McClenaghan C, Aryal P, Dong L et al. K2P channel gating mechanisms revealed by structures of TREK-2 and a complex with Prozac. Science 2015; 347: 1256-1259.
74. Bonnin A, Zhang L, Blakely RD, Levitt P. The SSRI citalopram affects fetal thalamic axon responsiveness to netrin-1 in vitro independently of SERT antagonism. Neuropsychopharmacology 2012; 37: 1879-1884.
75. Pi HJ, Hangya B, Kvitsiani D, Sanders JI, Huang ZJ, Kepecs A. Cortical interneurons that specialize in disinhibitory control. Nature 2013; 503: 521-524.
76. Lee S, Kruglikov I, Huang ZJ, Fishell G, Rudy B. A disinhibitory circuit mediates motor integration in the somatosensory cortex. Nat Neurosci 2013; 16: 1662-1670.
77. Bando Y, Irie K, Shimomura T, Umeshima H, Kushida Y, Kengaku M et al. Control of spontaneous Ca2+ transients is critical for neuronal maturation in the developing neocortex. Cereb Cortex; advance online publication, 11 August 2014; doi:10.1093/ cercor/bhu180.
78. Rampono J, Proud S, Hackett LP, Kristensen JH, Ilett KF. A pilot study of newer antidepressant concentrations in cord and maternal serum and possible effects in the neonate. Int J Neuropsychopharmacol 2004; 7: 329-334.
79. Mulder EJ, Ververs FF, de Heus R, Visser GH. Selective serotonin reuptake inhibitors affect neurobehavioral development in the human fetus. Neuropsychopharmacology 2011; 36: 1961-1971.
80. Rurak D, Lim K, Sanders A, Brain U, Riggs W, Oberlander TF. Third trimester fetal heart rate and doppler middle cerebral artery blood flow velocity characteristics during prenatal selective serotonin reuptake inhibitor (SSRI) exposure. Pediatr Res 2011; 70: 96-101.
81. Laine K, Heikkinen T, Ekblad U, Kero P. Effects of exposure to selective serotonin reuptake inhibitors during pregnancy on serotonergic symptoms in newborns and cord blood monoamine and prolactin concentrations. Arch Gen Psychiatry 2003; 60: 720-726.
82. Colvin L, Slack-Smith L, Stanley FJ, Bower C. Early morbidity and mortality following in utero exposure to selective serotonin reuptake inhibitors: a populationbased study in Western Australia. CNS Drugs 2012; 26: e1-e14.
83. Casper RC, Fleisher BE, Lee-Ancajas JC, Gilles A, Gaylor E, DeBattista A et al. Followup of children of depressed mothers exposed or not exposed to antidepressant drugs during pregnancy. J Pediatr 2003; 142: 402-408.
84. Oberlander TF, Warburton W, Misri S, Aghajanian J, Hertzman C. Effects of timing and duration of gestational exposure to serotonin reuptake inhibitor antidepressants: population-based study. Br J Psychiatry 2008; 192: 338-343.
85. Casper RC, Gilles AA, Fleisher BE, Baran J, Enns G, Lazzeroni LC. Length of prenatal exposure to selective serotonin reuptake inhibitor (SSRI) antidepressants: effects on neonatal adaptation and psychomotor development. Psychopharmacology (Berl) 2011; 217: 211-219.
86. El Marroun H, Jaddoe VW, Hudziak JJ, Roza SJ, Steegers EA, Hofman A et al. Maternal use of selective serotonin reuptake inhibitors, fetal growth, and risk of adverse birth outcomes. Arch Gen Psychiatry 2012; 69: 706-714.
87. Weikum WM, Oberlander TF, Hensch TK, Werker JF. Prenatal exposure to antidepressants and depressed maternal mood alter trajectory of infant speech perception. Proc Natl Acad Sci USA 2012; 109: 17221-17227.
88. Hanley GE, Brain U, Oberlander TF. Prenatal exposure to serotonin reuptake inhibitor antidepressants and childhood behavior. Pediatr Res 2015; 78: 174-180.
89. Weisskopf E, Fischer CJ, Bickle Graz M, Morisod Harari M, Tolsa JF, Claris O et al. Risk-benefit balance assessment of SSRI antidepressant use during pregnancy and lactation based on best available evidence. Expert Opin Drug Saf 2015; 1-15.