Bidirectional regulation of emotional memory by 5-HT 1B receptors involves hippocampal p11

Molecular Psychiatry

Volumn 18, Issue 10, 2013, Pages 1096-1105

  Eriksson, T M ^a   Alvarsson, A ^a   Stan, T L ^a   Zhang, X ^a   Hascup, K N ^a,b   Hascup, E R ^a,b   Kehr, J ^a   Gerhardt, G A ^b   Warner Schmidt, J ^c   Arango Lievano, M ^d   Kaplitt, M G ^d   Ogren S O ^a   Greengard, P ^c   Svenningsson, P ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF KENTUCKY   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

AAV; biosensor; MRS; novel object recognition; passive avoidance; S100A10

Indexed keywords

4 AMINOBUTYRIC ACID; ADAPTOR PROTEIN; GLUTAMATE RECEPTOR; GLUTAMIC ACID; PARVOVIRUS VECTOR; PROTEIN P11; SEROTONIN; SEROTONIN 1B AGONIST; SEROTONIN 1B RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOSENSOR; COGNITIVE DEFECT; CONTROLLED STUDY; DEPRESSION; EMOTION; FEMALE; GENETIC MODEL; GLUTAMATERGIC TRANSMISSION; HIPPOCAMPUS; IMMUNOBLOTTING; LONG TERM MEMORY; MALE; MEMORY; MEMORY DISORDER; MOUSE; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PASSIVE AVOIDANCE; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RECOGNITION; REGULATORY MECHANISM; SEROTONINERGIC TRANSMISSION; VIRAL GENE DELIVERY SYSTEM; WESTERN BLOTTING; WILD TYPE;

ANIMALS; ANNEXIN A2; AVOIDANCE LEARNING; DEPRESSION; DISEASE MODELS, ANIMAL; EMOTIONS; EXPLORATORY BEHAVIOR; FEMALE; GENES, REPORTER; GLUTAMIC ACID; HIPPOCAMPUS; MALE; MEMORY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHOSPHORYLATION; PRESYNAPTIC TERMINALS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PYRIDINES; REACTION TIME; RECEPTOR, SEROTONIN, 5-HT1B; RECEPTORS, AMPA; RECOMBINANT FUSION PROTEINS; S100 PROTEINS; SEROTONIN 5-HT1 RECEPTOR AGONISTS; SYNAPTIC TRANSMISSION; TRANSDUCTION, GENETIC;

EID: 84884670670     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2012.130     Document Type: Article

References (53)

1. Clark L, Chamberlain SR, Sahakian BJ. Neurocognitive mechanisms in depression: implications for treatment. Annu Rev Neurosci 2009; 32: 57-74.
2. MacQueen GM, Campbell S, McEwen BS, Macdonald K, Amano S, Joffe RT et al. Course of illness, hippocampal function, and hippocampal volume in major depression. Proc Natl Acad Sci USA 2003; 100: 1387-1392. (Pubitemid 36184011)
3. Roiser JP, Levy J, Fromm SJ, Nugent AC, Talagala SL, Hasler G et al. The effects of tryptophan depletion on neural responses to emotional words in remitted depression. Biol Psychiatry 2009; 66: 441-450.
4. Savitz J, Lucki I, Drevets WC.5-HT(1A) receptor function in major depressive disorder. Prog Neurobiol 2009; 88: 17-31.
5. Pittenger C, Duman RS. Stress, depression, and neuroplasticity: a convergence of mechanisms. Neuropsychopharmacology 2008; 33: 88-109. (Pubitemid 350191319)
6. Frodl T, Schaub A, Banac S, Charypar M, Jager M, Kummler P et al. Reduced hippocampal volume correlates with executive dysfunctioning in major depression. J Psychiatry Neurosci 2006; 31: 316-323.
7. Pfennig A, Littmann E, Bauer M. Neurocognitive impairment and dementia in mood disorders. J Neuropsychiatry Clin Neurosci 2007; 4: 373-382. (Pubitemid 350156094)
8. Goodwin GM. Symptom relief and facilitation of emotional processing. Eur Neuropsychopharmacol 2011; Suppl 4: S710-S715.
9. Pringle A, Browning M, Cowen PJ, Harmer CJ. A cognitive neuropsychological model of antidepressant drug action. Prog Neuropsychopharmacol Biol Psychiatry 2011; 35: 1586-1592.
10. Harmer CJ. Serotonin and emotional processing: does it help explain antidepressant drug action? Neuropharmacology 2008; 55: 1023-1028.
11. Harmer CJ, Cowen PJ, Goodwin GM. Efficacy markers in depression. J Psychopharmacol 2011; 9: 1148-1158.
12. Sambeth A, Blokland A, Harmer CJ, Kilkens TO, Nathan PJ, Porter RJ et al. Sex differences in the effect of acute tryptophan depletion on declarative episodic memory: a pooled analysis of nine studies. Neurosci Biobehav Rev 2007; 31: 516-529. (Pubitemid 46546436)
13. Lieben CK, van Oorsouw K, Deutz NE, Blokland A. Acute tryptophan depletion induced by a gelatin-based mixture impairs object memory but not affective behavior and spatial learning in the rat. Behav Brain Res 2004; 151: 53-64. (Pubitemid 38501428)
14. Uchida S, Umeeda H, Kitamoto A, Masushige S, Kida S. Chronic reduction in dietary tryptophan leads to a selective impairment of contextual fear memory in mice. Brain Res 2007; 1149: 149-156. (Pubitemid 46659897)
15. Ogren SO, Eriksson TM, Elvander-Tottie E, D'Addario C, Ekstrom JC, Svenningsson P et al. The role of 5-HT(1A) receptors in learning and memory. Behav Brain Res 2008; 195: 54-77.
16. Ohlander-Luttgen M, Madjid N, Schott PA, Sandin J,Ogren SO. Analysis of the role of the 5-HT1B receptor in spatial and aversive learning in the rat. Neuropsychopharmacology 2003; 28: 1642-1655. (Pubitemid 41070865)
17. Eriksson TM, Madjid N, Elvander-Tottie E, Stiedl O, Svenningsson P, Ogren SO. Blockade of 5-HT 1B receptors facilitates contextual aversive learning in mice by disinhibition of cholinergic and glutamatergic neurotransmission. Neuropharmacology 2008; 54: 1041-1050.
18. Stark KL, Hen R. Knockout Corner. Int J Neuropsychopharmacol 1999; 2: 145-150.
19. McDevitt RA, Hiroi R, Mackenzie SM, Robin NC, Cohn A, Kim JJ et al. Serotonin 1B autoreceptors originating in the caudal dorsal raphe nucleus reduce expression of fear and depression-like behavior. Biol Psychiatry 2011; 69: 780-787.
20. Murrough JW, Henry S, Hu J, Gallezot JD, Planeta-Wilson B, Neumaier JF et al. Reduced ventral striatal/ventral pallidal serotonin1B receptor binding potential in major depressive disorder. Psychopharmacology (Berl) 2011; 213: 547-553.
21. Anisman H, Du L, Palkovits M, Faludi G, Kovacs GG, Szontagh-Kishazi P et al. Serotonin receptor subtype and p11 mRNA expression in stress-relevant brain regions of suicide and control subjects. J Psychiatry Neurosci 2008; 33: 131-141. (Pubitemid 351441383)
22. Svenningsson P, Chergui K, Rachleff I, Flajolet M, Zhang X, El Yacoubi M et al. Alterations in 5-HT1BR function by p11 in depression-like states. Science 2006; 311: 77-80. (Pubitemid 43063061)
23. Svenningsson P, Greengard P. p11 (S100A10)-an inducible adaptor protein that modulates neuronal functions. Curr Opin Pharmacol 2007; 7: 27-32.
24. Warner-Schmidt JL, Flajolet M, Maller A, Chen EY, Qi H, Svenningsson P et al. Role of p11 in cellular and behavioral effects of 5-HT4 receptor stimulation. J Neurosci 2009; 29: 1937-1946.
25. Alexander B, Warner-Schmidt J, Eriksson T, Tamminga C, Arango-Lievano M, Ghose S et al. Reversal of depressed behaviors in mice by p11 gene therapy in the nucleus accumbens. Sci Transl Med 2010; 2: 54ra76.
26. Zhang X, Andren PE, Greengard P, Svenningsson P. Evidence for a role of the 5-HT1BR and its adaptor protein, p11, in L-DOPA treatment of an animal model of Parkinsonism. Proc Natl Acad Sci USA 2008; 105: 2163-2168. (Pubitemid 351439482)
27. Shanahan NA, Holick Pierz KA, Masten VL, Waeber C, Ansorge M et al. Chronic reductions in serotonin transporter function prevent 5-HT1B-induced behavioral effects in mice. Biol Psychiatry 2009; 65: 401-408.
28. Baarendse PJ, van Grootheest G, Jansen RF, Pieneman AW, Ogren SO, Verhage M et al. Differential involvement of the dorsal hippocampus in passive avoidance in C57bl/6J and DBA/2J mice. Hippocampus 2008; 18: 11-19.
29. Svenningsson P, Le Moine C, Aubert I, Burbaud P, Fredholm BB, Bloch B. Cellular distribution of adenosine A2A receptor mRNA in the primate striatum. J Comp Neurol 1998; 399: 229-240. (Pubitemid 28376468)
30. Eriksson TM, Delagrange P, Spedding M, Popoli M, MatheAA, Ogren SO et al. Emotional memory impairments in a genetic rat model of depression: involvement of 5-HT/MEK/Arc signaling in restoration. Mol Psychiatry 2012; 2: 173-184.
31. Bao X, Pal R, Hascup KN, Wang Y, Wang WT, Xu W et al. Transgenic expression of Glud1 (glutamate dehydrogenase 1) in neurons: in vivo model of enhanced glutamate release, altered synaptic plasticity, and selective neuronal vulnerability. J Neurosci 2009; 29: 13929-13944.
32. Hascup KN, Hascup ER, Pomerleau F, Huettl P, Gerhardt GA. Second-by-second measures of L-glutamate in the prefrontal cortex and striatum of freely moving mice. J Pharmacol Exp Ther 2008; 324: 725-731. (Pubitemid 351185870)
33. Thomas TC, Grandy DK, Gerhardt GA, Glaser PE. Decreased dopamine D4 receptor expression increases extracellular glutamate and alters its regulation in mouse striatum. Neuropsychopharmacology 2009; 34: 436-445.
34. Ross JM, Oberg J, Brene S, Coppotelli G, Terzioglu M, Pernold K et al. High brain lactate is a hallmark of aging and caused by a shift in the lactate dehydrogenase A/B ratio. Proc Natl Acad Sci USA 2010; 107: 20087-20092.
35. LeDoux JE. Emotion circuits in the brain. Annu Rev Neurosci 2000; 23: 155-184.
36. LeDoux JE, Muller J. Emotional memory and psychopathology. Philos Trans R Soc Lond B Biol Sci 1997; 352: 1719-1726. (Pubitemid 28000466)
37. Burwell RD, Saddoris MP, Bucci DJ, Wiig KA. Corticohippocampal contributions to spatial and contextual learning. J Neurosci 2004; 24: 3826-3236.
38. Cahill L, McGaugh JL. Mechanisms of emotional arousal and lasting declarative memory. Trends Neurosci 1998; 21: 294-299. (Pubitemid 28293639)
39. McGaugh JL. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci 2004; 27: 1-28. (Pubitemid 39050395)
40. Fendt M, Fanselow MS. The neuroanatomical and neurochemical basis of conditioned fear. Neurosci Biobehav Rev 1999; 23: 743-760. (Pubitemid 29282023)
41. Holland PC, Bouton ME. Hippocampus and context in classical conditioning. Curr Opin Neurobiol 1999; 9: 195-202. (Pubitemid 29201792)
42. Egeland M, Warner-Schmidt J, Greengard P, Svenningsson P. Neurogenic effects of fluoxetine are attenuated in p11 (S100A10) knockout mice. Biol Psychiatry 2010; 67: 1048-1056.
43. Hu XJ, Wang FH, Stenfors C, Ogren SO, Kehr J. Effects of the 5-HT1BR antagonist NAS-181 on extracellular levels of acetylcholine, glutamate and GABA in the frontal cortex and ventral hippocampus of awake rats: a microdialysis study. Eur Neuropsychopharmacol 2007a; 17: 580-586. (Pubitemid 47078998)
44. Mlinar B, Falsini C, Corradetti R. Pharmacological characterization of 5-HT1B receptor-mediated inhibition of local excitatory synaptic transmission in the CA1 region of rat hippocampus. Br J Pharmacol 2003; 138: 71-80. (Pubitemid 36194205)
45. Winterer J, Stempel AV, Dugladze T, Foldy C, Maziashvili N, Zivkovic AR et al. Celltype-specific modulation of feedback inhibition by serotonin in the hippocampus. J Neurosci 2011; 31: 8464-8475.
46. Peddie CJ, Davies HA, Colyer FM, Stewart MG, Rodrguez JJ. Dendritic colocalisation of serotonin1B receptors and the glutamate NMDA receptor subunit NR1 within the hippocampal dentate gyrus: an ultrastructural study. J Chem Neuroanat 2008; 36: 17-26.
47. Timmerman W, Westerink BH. Brain microdialysis of GABA and glutamate: what does it signify? Synapse 1997; 27: 242-261. (Pubitemid 27430673)
48. Lee HK, Takamiya K, Han JS, Man H, Kim CH, Rumbaugh G et al. Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory. Cell 2003; 112: 631-643. (Pubitemid 36331776)
49. Hu H, Real E, Takamiya K, Kang MG, Ledoux J, Huganir RL et al. Emotion enhances learning via norepinephrine regulation of AMPA-receptor trafficking. Cell 2007b; 131: 160-173. (Pubitemid 47498536)
50. Sanacora G, Gueorguieva R, Epperson CN, Wu YT, Appel M, Rothman DL et al. Subtype-specific alterations of GABA and glutamate in major depression. Arch Gen Psychiatry 2004; 61: 705e713.
51. Luscher B, Shen Q, Sahir N. The GABAergic deficit hypothesis of major depressive disorder. Mol Psychiatry 2011; 16: 383-406.
52. Rajkowska G, O'Dwyer G, Teleki Z, Stockmeier CA, Miguel-Hidalgo JJ. GABAergic neurons immunoreactive for calcium binding proteins are reduced in the prefrontal cortex in major depression. Neuropsychopharmacology 2007; 32: 471-482. (Pubitemid 46106953)
53. Franklin KBJ, Paxinos G. The Mouse Brain in Stereotaxic coordinates. Academic: San Diego, 1997.