Serotonin 1A receptors in human and monkey prefrontal cortex are mainly expressed in pyramidal neurons and in a GABAergic interneuron subpopulation: Implications for schizophrenia and its treatment

Journal of Neurochemistry

Volumn 107, Issue 2, 2008, Pages 488-496

  De Almeida, Julián ^a,b   Mengod, Guadalupe ^a,b  

^a INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

Author keywords

Calbindin; Co localization; Interneurons; Parvalbumin; Pyramidal neurons; Serotonin 1A

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; MESSENGER RNA; SEROTONIN 1A RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL POPULATION; CONTROLLED STUDY; IN SITU HYBRIDIZATION; MONKEY; NONHUMAN; PHENOTYPE; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; SCHIZOPHRENIA;

AGED; ANIMALS; AUTORADIOGRAPHY; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; HUMANS; INTERNEURONS; MACACA FASCICULARIS; MIDDLE AGED; PARVALBUMINS; POSTMORTEM CHANGES; PREFRONTAL CORTEX; PYRAMIDAL CELLS; RECEPTOR, SEROTONIN, 5-HT1A; RNA, MESSENGER; SCHIZOPHRENIA; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1;

PRIMATES;

EID: 53149086275     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05649.x     Document Type: Article

References (49)

1. de Almeida J. Mengod G. (2007) Quantitative analysis of glutamatergic and GABAergic neurons expressing 5-HT(2A) receptors in human and monkey prefrontal cortex. J. Neurochem. 103, 475 486.
2. Amargós-Bosch M., Bortolozzi A., Puig M. V., Serrats J., Adell A., Celada P., Toth M., Mengod G. Artigas F. (2004) Co-expression and in vivo interaction of serotonin1A and serotonin2A receptors in pyramidal neurons of prefrontal cortex. Cereb. Cortex 14, 281 299.
3. Araneda R. Andrade R. (1991) 5-Hydroxytryptamine2 and 5-hydroxytryptamine 1A receptors mediate opposing responses on membrane excitability in rat association cortex. Neuroscience 40, 399 412.
4. Artigas F., Romero L., de Montigny C. Blier P. (1996) Acceleration of the effect of selected antidepressant drugs in major depression by 5-HT1A antagonists. Trends Neurosci. 19, 378 383.
5. Auclair A. L., Galinier A., Besnard J., Newman-Tancredi A. Depoortere R. (2007) Putative antipsychotics with pronounced agonism at serotonin 5-HT1A and partial agonist activity at dopamine D2 receptors disrupt basal PPI of the startle reflex in rats. Psychopharmacology (Berl) 193, 45 54.
6. Aznar S., Qian Z., Shah R., Rahbek B. Knudsen G. M. (2003) The 5-HT1A serotonin receptor is located on calbindin- and parvalbumin-containing neurons in the rat brain. Brain Res. 959, 58 67.
7. Bantick R. A., Deakin J. F. Grasby P. M. (2001) The 5-HT1A receptor in schizophrenia: a promising target for novel atypical neuroleptics? J. Psychopharmacol. 15, 37 46.
8. Bantick R. A., Montgomery A. J., Bench C. J., Choudhry T., Malek N., McKenna P. J., Quested D. J., Deakin J. F. Grasby P. M. (2004) A positron emission tomography study of the 5-HT1A receptor in schizophrenia and during clozapine treatment. J. Psychopharmacol. 18, 346 354.
9. Carrel D., Hamon M. Darmon M. (2006) Role of the C-terminal di-leucine motif of 5-HT1A and 5-HT1B serotonin receptors in plasma membrane targeting. J. Cell Sci. 119, 4276 4284.
10. Chou Y. H., Halldin C. Farde L. (2003) Occupancy of 5-HT1A receptors by clozapine in the primate brain: a PET study. Psychopharmacology (Berl) 166, 234 240.
11. Cruz D. A., Eggan S. M., Azmitia E. C. Lewis D. A. (2004) Serotonin1A receptors at the axon initial segment of prefrontal pyramidal neurons in schizophrenia. Am. J. Psychiatry 161, 739 742.
12. Cuisiat S., Bourdiol N., Lacharme V., Newman-Tancredi A., Colpaert F. Vacher B. (2007) Towards a new generation of potential antipsychotic agents combining D2 and 5-HT1A receptor activities. J. Med. Chem. 50, 865 876.
13. De Vry J. (1995) 5-HT1A receptor agonists: recent developments and controversial issues. Psychopharmacology (Berl) 121, 1 26.
14. DeFelipe J. (1997) Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex. J. Chem. Neuroanat. 14, 1 19.
15. DeFelipe J., Arellano J. I., Gomez A., Azmitia E. C. Munoz A. (2001) Pyramidal cell axons show a local specialization for GABA and 5-HT inputs in monkey and human cerebral cortex. J. Comp. Neurol. 433, 148 155.
16. Diaz-Mataix L., Scorza M. C., Bortolozzi A., Toth M., Celada P. Artigas F. (2005) Involvement of 5-HT1A receptors in prefrontal cortex in the modulation of dopaminergic activity: role in atypical antipsychotic action. J. Neurosci. 25, 10831 10843.
17. Diaz-Mataix L., Artigas F. Celada P. (2006) Activation of pyramidal cells in rat medial prefrontal cortex projecting to ventral tegmental area by a 5-HT1A receptor agonist. Eur. Neuropsychopharmacol. 16, 288 296.
18. Harder J. A. Ridley R. M. (2000) The 5-HT1A antagonist, WAY 100 635, alleviates cognitive impairments induced by dizocilpine (MK-801) in monkeys. Neuropharmacology 39, 547 552.
19. Ichikawa J., Ishii H., Bonaccorso S., Fowler W. L., O'Laughlin I. A. Meltzer H. Y. (2001) 5-HT(2A) and D(2) receptor blockade increases cortical DA release via 5-HT(1A) receptor activation: a possible mechanism of atypical antipsychotic-induced cortical dopamine release. J. Neurochem. 76, 1521 1531.
20. Jolimay N., Franck L., Langlois X., Hamon M. Darmon M. (2000) Dominant role of the cytosolic C-terminal domain of the rat 5-HT1B receptor in axonal-apical targeting. J. Neurosci. 20, 9111 9118.
21. Landry M., Holmberg K., Zhang X. Hokfelt T. (2000) Effect of axotomy on expression of NPY, galanin, and NPY Y1 and Y2 receptors in dorsal root ganglia and the superior cervical ganglion studied with double-labeling in situ hybridization and immunohistochemistry. Exp. Neurol. 162, 361 384.
22. Marazziti D., Marracci S., Palego L., Rotondo A., Mazzanti C., Nardi I., Ladinsky H., Giraldo E., Borsini F. Cassano G. B. (1994) Localization and gene expression of serotonin 1A (5HT1A) receptors in human brain postmortem. Brain Res. 658, 55 59.
23. Martin-Ruiz R., Puig M. V., Celada P., Shapiro D. A., Roth B. L., Mengod G. Artigas F. (2001) Control of serotonergic function in medial prefrontal cortex by serotonin-2A receptors through a glutamate-dependent mechanism. J. Neurosci. 21, 9856 9866.
24. Meltzer H. Y. (1999) The role of serotonin in antipsychotic drug action. Neuropsychopharmacology 21, 106S 115S.
25. Meltzer H. Y., Li Z., Kaneda Y. Ichikawa J. (2003) Serotonin receptors: their key role in drugs to treat schizophrenia. Prog. Neuropsychopharmacol. Biol. Psychiatry 27, 1159 1172.
26. Mengod G., Vilaró M. T., Raurich A., López-Giménez J. F., Cortés R. Palacios J. M. (1996) 5-HT receptors in mammalian brain: receptor autoradiography and in situ hybridization studies of new ligands and newly identified receptors. Histochem. J. 28, 747 758.
27. Millan M. J. (2000) Improving the treatment of schizophrenia: focus on serotonin (5-HT)(1A) receptors. J. Pharmacol. Exp. Ther. 295, 853 861.
28. Misane I. Ogren S. O. (2003) Selective 5-HT1A antagonists WAY 100635 and NAD-299 attenuate the impairment of passive avoidance caused by scopolamine in the rat. Neuropsychopharmacology 28, 253 264.
29. Moghaddam B. (1994) Preferential activation of cortical dopamine neurotransmission by clozapine: functional significance. J. Clin. Psychiatry 55 (Suppl B 27 29.
30. Newman-Tancredi A., Chaput C., Verriele L. Millan M. J. (1996) Clozapine is a partial agonist at cloned, human serotonin 5-HT1A receptors. Neuropharmacology 35, 119 121.
31. Newman-Tancredi A., Gavaudan S., Conte C., Chaput C., Touzard M., Verriele L., Audinot V. Millan M. J. (1998) Agonist and antagonist actions of antipsychotic agents at 5-HT1A receptors: a [35S]GTPgammaS binding study. Eur. J. Pharmacol. 355, 245 256.
32. Newman-Tancredi A., Verriele L., Touzard M. Millan M. J. (2001) Efficacy of antipsychotic agents at human 5-HT(1A) receptors determined by [3H]WAY100,635 binding affinity ratios: relationship to efficacy for G-protein activation. Eur. J. Pharmacol. 428, 177 184.
33. Nordberg A. (1992) Neuroreceptor changes in Alzheimer disease. Cerebrovasc. Brain Metab. Rev. 4, 303 328.
34. Palchaudhuri M. Flugge G. (2005) 5-HT1A receptor expression in pyramidal neurons of cortical and limbic brain regions. Cell Tissue Res. 321, 159 172.
35. Paxinos G., Huang X.-F. Toga A. W. (2000) The Rhesus Monkey Brain. Academic Press, San Diego.
36. Pazos A. Palacios J. M. (1985) Quantitative autoradiographic mapping of serotonin receptors in the rat brain. I. Serotonin-1 receptors. Brain Res. 346, 205 230.
37. Pazos A., Probst A. Palacios J. M. (1987) Serotonin receptors in the human brain - III. Autoradiographic mapping of serotonin-1 receptors. Neuroscience 21, 97 122.
38. Pompeiano M., Palacios J. M. Mengod G. (1992) Distribution and cellular localization of mRNA coding for 5-HT1A receptor in the rat brain: correlation with receptor binding. J. Neurosci. 12, 440 453.
39. Puig M. V., Artigas F. Celada P. (2005) Modulation of the activity of pyramidal neurons in rat prefrontal cortex by raphe stimulation in vivo: involvement of serotonin and GABA. Cereb. Cortex 15, 1 14.
40. Riad M., Garcia S., Watkins K. C., Jodoin N., Doucet E., Langlois X., el Mestikawy S., Hamon M. Descarries L. (2000) Somatodendritic localization of 5-HT1A and preterminal axonal localization of 5-HT1B serotonin receptors in adult rat brain. J. Comp. Neurol. 417, 181 194.
41. Sakaue M., Somboonthum P., Nishihara B., Koyama Y., Hashimoto H., Baba A. Matsuda T. (2000) Postsynaptic 5-hydroxytryptamine(1A) receptor activation increases in vivo dopamine release in rat prefrontal cortex. Br. J. Pharmacol. 129, 1028 1034.
42. Santana N., Bortolozzi A., Serrats J., Mengod G. Artigas F. (2004) Expression of serotonin1A and serotonin2A receptors in pyramidal and GABAergic neurons of the rat prefrontal cortex. Cereb. Cortex 14, 1100 1109.
43. Schmitz G. G., Walter T., Seibl R. Kessler C. (1991) Nonradioactive labeling of oligonucleotides in vitro with the hapten digoxigenin by tailing with terminal transferase. Anal. Biochem. 192, 222 231.
44. Serrats J., Artigas F., Mengod G. Cortés R. (2003) GABAB receptor mRNA in the raphe nuclei: co-expression with serotonin transporter and glutamic acid decarboxylase. J. Neurochem. 84, 743 752.
45. Smiley J. F. Goldman-Rakic P. S. (1996) Serotonergic axons in monkey prefrontal cerebral cortex synapse predominantly on interneurons as demonstrated by serial section electron microscopy. J. Comp. Neurol. 367, 431 443.
46. Stockmeier C. A., Shapiro L. A., Dilley G. E., Kolli T. N., Friedman L. Rajkowska G. (1998) Increase in serotonin-1A autoreceptors in the midbrain of suicide victims with major depression-postmortem evidence for decreased serotonin activity. J. Neurosci. 18, 7394 7401.
47. Tomiyama M., Palacios J. M., Cortés R., Vilaró M. T. Mengod G. (1997) Distribution of AMPA receptor subunit mRNAs in the human basal ganglia: an in situ hybridization study. Mol. Brain Res. 46, 281 289.
48. Wilson M. A. Molliver M. E. (1991) The organization of serotonergic projections to cerebral cortex in primates: regional distribution of axon terminals. Neuroscience 44, 537 553.
49. Zaitsev A. V., Gonzalez-Burgos G., Povysheva N. V., Kroner S., Lewis D. A. Krimer L. S. (2005) Localization of calcium-binding proteins in physiologically and morphologically characterized interneurons of monkey dorsolateral prefrontal cortex. Cereb. Cortex 15, 1178 1186.