Disrupting the melanin-concentrating hormone receptor 1 in mice leads to cognitive deficits and alterations of NMDA receptor function.

Adamantidis, Antoine; Thomas, Elizabeth; Foidart, Agnès; Tyhon, Amélie; Coumans, Bernard; Minet, Arlette; Tirelli, Ezio; Seutin, Vincent; Grisar, Thierry; Lakaye, Bernard

doi:10.1111/j.1460-9568.2005.04100.x

Article (Scientific journals)

Disrupting the melanin-concentrating hormone receptor 1 in mice leads to cognitive deficits and alterations of NMDA receptor function.

Adamantidis, Antoine; Thomas, Elizabeth; Foidart, Agnès et al.

2005 • In European Journal of Neuroscience, 21 (10), p. 2837-44

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/5144

DOI
10.1111/j.1460-9568.2005.04100.x

PubMed
15926931

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

AdamantadisEtal2005.pdf

Publisher postprint (329.74 kB)

Request a copy

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Animals; Anxiety; Avoidance Learning/physiology; Electroshock; Exploratory Behavior; Gene Deletion; Habituation, Psychophysiologic; Hippocampus/drug effects/physiology; In Situ Hybridization; Mice; Mice, Knockout; N-Methylaspartate/pharmacology; Pyramidal Cells/drug effects/physiology; Receptors, Somatostatin/deficiency/genetics; Tetrodotoxin/pharmacology

Abstract :

[en] In order to investigate the physiological properties of the melanin-concentrating hormone (MCH) we have generated and used mice from which the MCH receptor 1 gene was deleted (MCHR1(Neo/Neo) mice). Complementary experimental approaches were used to investigate alterations in the learning and memory processes of our transgenic model. The ability of the knockout strain to carry out the inhibitory passive avoidance test was found to be considerably impaired although no significant differences were observed in anxiety levels. This impaired cognitive property prompted us to explore modifications in N-methyl D-aspartate (NMDA) responses in the hippocampus. Intracellular recordings of CA1 pyramidal neurons in hippocampal slices from the MCHR1(Neo/Neo) mice revealed significantly decreased NMDA responses. Finally, using in situ hybridization we found a 15% reduction in NMDAR1 subunit in the CA1 region. These results show for the first time a possible role for MCH in the control of the function of the NMDA receptor.

Disciplines :

Pharmacy, pharmacology & toxicology

Author, co-author :

Adamantidis, Antoine ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biochimie et physiologie humaine et pathologique

Thomas, Elizabeth

Foidart, Agnès ; Université de Liège - ULiège > Services généraux (Faculté de médecine) > Service administratif de la Faculté (Médecine)

Tyhon, Amélie ; Université de Liège - ULiège > Département des sciences cognitives > Neuroscience comportementale et psychopharmacologie expér.

Coumans, Bernard ; Université de Liège - ULiège > CNCM/ Centre fac. de rech. en neurobiologie cell. et moléc.

Minet, Arlette ; Centre Hospitalier Universitaire de Liège - CHU > Neurologie Sart Tilman

Tirelli, Ezio ; Université de Liège - ULiège > Département des sciences cognitives > Neuroscience comportementale et psychopharmacologie expér.

Seutin, Vincent ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Pharmacologie

Grisar, Thierry ; Centre Hospitalier Universitaire de Liège - CHU > Neurologie Sart Tilman

Lakaye, Bernard ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biochimie et physiologie humaine et pathologique

Language :

English

Title :

Disrupting the melanin-concentrating hormone receptor 1 in mice leads to cognitive deficits and alterations of NMDA receptor function.

Publication date :

2005

Journal title :

European Journal of Neuroscience

ISSN :

0953-816X

eISSN :

1460-9568

Publisher :

Blackwell Science, Paris, France

Volume :

Issue :

Pages :

2837-44

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 16 April 2010

Statistics

Number of views

54 (1 by ULiège)

Number of downloads

0 (0 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Abbott, C.R., Kennedy, A.R., Wren, A.M., Rossi, M., Murphy, K.G., Seal, L.J., Todd, J.F., Ghatei, M.A., Small, C.J. & Bloom, S.R. (2003) Identification of hypothalamic nuclei involved in the orexigenic effect of melanin-concentrating hormone. Endocrinology, 144, 3943-3949.
An, S., Cutler, G., Zhao, J.J., Huang, S.G., Tian, H., Li, W., Liang, L., Rich, M., Du Bakleh, A.J., Chen, J.L. & Dai, K. (2001) Identification and characterization of a melanin-concentrating hormone receptor. Proc. Natl Acad. Sci. USA, 98, 7576-7581.
Astrand, A., Bohlooly, Y.M., Larsdotter, S., Mahlapuu, M., Andersen, H., Tornell, J., Ohlsson, C., Snaith, M. & Morgan, D.G. (2004) Mice lacking the melanin concentrating hormone receptor 1 demonstrate increased heart rate associated with altered autonomic activity. Am. J. Physiol. Regul. Integr. Comp. Physiol., in press.
Bachner, D., Kreienkamp, H.J. & Richter, D. (2002) MIZIP, a highly conserved, vertebrate specific melanin-concentrating hormone receptor 1 interacting zinc-finger protein. FEBS Lett., 526, 124-128.
Bachner, D., Kreienkamp, H., Weise, C., Buck, F. & Richter, D. (1999) Identification of melanin concentrating hormone (MCH) as the natural ligand for the orphan somatostatin-like receptor 1 (SLC-1). FEBS Lett., 457, 522-524.
Bernaerts, P., Lamberty, Y. & Tirelli, E. (2004) Histamine H3 antagonist thioperamide dose-dependently enhances memory consolidation and reverses amnesia induced by dizocilpine or scopolamine in a one-trial inhibitory avoidance task in mice. Behav. Brain Res., 154, 211-219.
Bernaerts, P. & Tirelli, E. (2003) Facilitatory effect of the dopamine D4 receptor agonist PD168,077 on memory consolidation of an inhibitory avoidance learned response in C57BL/6J mice. Behav. Brain Res., 142, 41-52.
Bittencourt, J.C., Presse, F., Arias, C., Peto, C., Vaughan, J., Nahon, J.L., Vale, W. & Sawchenko, P.E. (1992) The melanin-concentrating hormone system of the rat brain: an immuno- and hybridization histochemical characterization. J. Comp. Neurol., 319, 218-245.
Chambers, J., Ames, R.S., Bergsma, D., Muir, A., Fitzgerald, L.R., Hervieu, G., Dytko, G.M., Foley, J.J., Martin, J., Liu, W.S., Park, J., Ellis, C., Ganguly, S., Konchar, S., Cluderay, J., Leslie, R., Wilson, S. & Sarau, H.M. (1999) Melanin-concentrating hormone is the cognate ligand for the orphan G-protein-coupled receptor SLC-1. Nature, 400, 261-265.
Chen, Y., Hu, C., Hsu, C.K., Zhang, Q., Bi, C., Asnicar, M., Hsiung, H.M., Fox, N., Slieker, L.J., Yang, D.D., Heiman, M.L. & Shi, Y. (2002) Targeted disruption of the melanin-concentrating hormone receptor-1 results in hyperphagia and resistance to diet-induced obesity. Endocrinology, 143, 2469-2477.
Della-Zuana, O., Presse, F., Ortola, C., Duhault, J., Nahon, J.L. & Levens, N. (2002) Acute and chronic administration of melanin-concentrating hormone enhances food intake and body weight in Wistar and Sprague-Dawley rats. Int. J. Obes. Relat. Metab. Disord., 26, 1289-1295.
Fried, S., O'Neill, K. & Hawes, B.E. (2002) Cloning and characterization of rhesus monkey MCH-R1 and MCH-R2. Peptides, 23, 1401-1408.
Fukaya, M., Kato, A., Lovett, C., Tonegawa, S. & Watanabe, M. (2003) Retention of NMDA receptor NR2 subunits in the lumen of endoplasmic reticulum in targeted NR1 knockout mice. Proc. Natl Acad. Sci. USA, 100, 4855-4860.
Gao, X.B. & van den Pol, A.N. (2002) Melanin-concentrating hormone depresses L-, N-, and P/Q-type voltage-dependent calcium channels in rat lateral hypothalamic neurons. J. Physiol. (Lond.), 542, 273-286.
Gomori, A., Ishihara, A., Ito, M., Mashiko, S., Matsushita, H., Yumoto, M., Tanaka, T., Tokita, S., Moriya, M., Iwaasa, H. & Kanatani, A. (2003) Chronic intracerebroventricular infusion of MCH causes obesity in mice. Melanin-concentrating hormone. Am. J. Physiol. Endocrinol. Metab., 284, E583-E588.
Gonzalez, M.I., Vaziri, S. & Wilson, C.A. (1996) Behavioral effects of alpha-MSH and MCH after central administration in the female rat. Peptides, 17, 171-177.
Griffond, B. & Baker, B.I. (2002) Cell and molecular cell biology of melanin-concentrating hormone. Int. Rev. Cytol., 213, 233-277.
Hervieu, G. (2003) Melanin-concentrating hormone functions in the nervous system: food intake and stress. Expert Opin. Ther. Targets, 7, 495-511.
Hervieu, G.J., Cluderay, J.E., Harrison, D., Meakin, J., Maycox, P., Nasir, S. & Leslie, R.A. (2000) The distribution of the mRNA and protein products of the melanin-concentrating hormone (MCH) receptor gene, slc-1, in the central nervous system of the rat. Eur. J. Neurosci., 12, 1194-1216.
Hill, J., Duckworth, M., Murdock, P., Rennie, G., Sabido-David, C., Ames, R.S., Szekeres, P., Wilson, S., Bergsma, D.J., Gloger, I.S., Levy, D.S., Chambers, J.K. & Muir, A.I. (2001) Molecular cloning and functional characterization of MCH2, a novel human MCH receptor. J. Biol. Chem., 276, 20125-20129.
Izquierdo, I. & Medina, J.H. (1997) Memory formation: the sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol. Learn. Mem., 68, 285-316.
Kim, M. & McGaugh, J.L. (1992) Effects of intra-amygdala injections of NMDA receptor antagonists on acquisition and retention of inhibitory avoidance. Brain Res., 585, 35-48.
Lakaye, B., Adamantidis, A., Coumans, B. & Grisar, T. (2004) Promoter characterization of the mouse melanin-concentrating hormone receptor 1. Biochim. Biophys. Acta, 1678, 1-6.
Lakaye, B., de Borman, B., Minet, A., Arckens, L., Vergnes, M., Marescaux, C. & Grisar, T. (2000) Increased expression of mRNA encoding ferritin heavy chain in brain structures of a rat model of absence epilepsy. Exp. Neurol., 162, 112-120.
Lakaye, B., Minet, A., Zorzi, W. & Grisar, T. (1998) Cloning of the rat brain cDNA encoding for the SLC-1 G protein-coupled receptor reveals the presence of an intron in the gene. Biochim. Biophys. Acta, 1401, 216-220.
Lembo, P.M., Grazzini, E., Cao, J., Hubatsch, D.A., Pelletier, M., Koffert, C., St-Onge, S., Pou, C., Labrecque, J., Groblewski, T., O'Donnell, D., Payza, K., Ahmad, S. & Walker, P. (1999) The receptor for the orexigenic peptide melanin-concentrating hormone is a G-protein-coupled receptor. Nat. Cell Biol., 1, 267-271.
Ludwig, D.S., Tritos, N.A., Mastaitis, J.W., Kulkarni, R., Kokkotou, E., Elmquist, J., Lowell, B., Flier, J.S. & Maratos-Flier, E. (2001) Melanin-concentrating hormone overexpression in transgenic mice leads to obesity and insulin resistance. J. Clin. Invest., 107, 379-386.
Macdonald, D., Murgolo, N., Zhang, R., Durkin, J.P., Yao, X., Strader, C.D. & Graziano, M.P. (2000) Molecular characterization of the melanin-concentrating hormone/receptor complex: identification of critical residues involved in binding and activation. Mol. Pharmacol., 58, 217-225.
Manabe, T., Noda, Y., Mamiya, T., Katagiri, H., Houtani, T., Nishi, M., Noda, T., Takahashi, T., Sugimoto, T., Nabeshima, T. & Takeshima, H. (1998) Facilitation of long-term potentiation and memory in mice lacking nociceptin receptors. Nature, 394, 577-581.
Marsh, D.J., Weingarth, D.T., Novi, D.E., Chen, H.Y., Trumbauer, M.E., Chen, A.S., Guan, X.M., Jiang, M.M., Feng, Y., Camacho, R.E., Shen, Z. & Frazier, E.G., YuH., Metzger, J.M., Kuca, S.J., Shearman, L.P., Gopal-Truter, S., MacNeil, D.J., Strack, A.M., MacIntyre, D.E., Van der Ploeg, L.H. & Qian, S. (2002) Melanin-concentrating hormone 1 receptor-deficient mice are lean, hyperactive, and hyperphagic and have altered metabolism. Proc. Natl. Acad. Sci. USA, 99, 3240-3245.
McGaugh, J.L. (2004) The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu. Rev. Neurosci., 27, 1-28.
Monzon, M.E., de Souza, M.M., Izquierdo, L.A., Izquierdo, I., Barros, D.M. & de Barioglio, S.R. (1999) Melanin-concentrating hormone (MCH) modifies memory retention in rats. Peptides, 20, 1517-1519.
Myers, J.L. & Well, A.D. (2003) Research Design and Statistical Analysis, 2nd edn. Lawrence Erlbaum Associates, Mahwah, New Jersey.
Nahon, J.L. (1994) The melanin-concentrating hormone: from the peptide to the gene. Crit. Rev. Neurobiol., 8, 221-262.
Nahon, J.L., Presse, F., Bittencourt, J.C., Sawchenko, P.E. & Vale, W. (1989) The rat melanin-concentrating hormone messenger ribonucleic acid encodes multiple putative neuropeptides coexpressed in the dorsolateral hypothalamus. Endocrinology, 125, 2056-2065.
Ozawa, S., Kamiya, H. & Tsuzuki, K. (1998) Glutamate receptors in the mammalian central nervous system. Prog. Neurobiol., 54, 581-618.
Parker, D. & Grillner, S. (1999) Long-lasting substance-P-mediated modulation of NMDA-induced rhythmic activity in the lamprey locomotor network involves separate RNA- and protein-synthesis-dependent stages. Eur. J. Neurosci., 11, 1515-1522.
Pissios, P., Trombly, D.J., Tzameli, I. & Maratos-Flier, E. (2003) Melanin-concentrating hormone receptor 1 activates extracellular signal-regulated kinase and synergizes with G (s)-coupled pathways. Endocrinology, 144, 3514-3523.
Pittaluga, A., Feligioni, M., Longordo, F., Arvigo, M. & Raiteri, M. (2004) Somatostatin-induced activation and upregulation of NMDA receptor function: mediation through CaMKII, PLC, PKC and Src in hippocampal noradrenergic nerve endings. J. Pharmacol. Exp. Ther., in press.
Presse, F., Hervieu, G., Imaki, T., Sawchenko, P.E., Vale, W. & Nahon, J.L. (1992) Rat melanin-concentrating hormone messenger ribonucleic acid expression: marked changes during development and after stress and glucocorticoid stimuli. Endocrinology, 131, 1241-1250.
Qu, D., Ludwig, D.S., Gammeltoft, S., Piper, M., Pelleymounter, M.A., Cullen, M.J., Mathes, W.F., Przypek, R., Kanarek, R. & Maratos-Flier, E. (1996) A role for melanin-concentrating hormone in the central regulation of feeding behaviour. Nature, 380, 243-247.
Rodriguez, M., Beauverger, P., Naime, I., Rique, H., Ouvry, C., Souchaud, S., Dromaint, S., Nagel, N., Suply, T., Audinot, V., Boutin, J.A. & Galizzi, J.P. (2001) Cloning and molecular characterization of the novel human melanin-concentrating hormone receptor MCH2. Mol. Pharmacol., 60, 632-639.
Rubin, M.A., Stiegemeier, J.A., Volkweis, M.A., Oliveira, D.M., Fenili, A.C., Boemo, R.L., Jurach, A. & Mello, C.F. (2001) Intra-amygdala spermidine administration improves inhibitory avoidance performance in rats. Eur. J. Pharmacol., 423, 35-39.
Sailer, A.W., Sano, H., Zeng, Z., McDonald, T.P., Pan, J., Pong, S.S., Feighner, S.D., Tan, C.P., Fukami, T., Iwaasa, H., Hreniuk, D.L., Morin, N.R., Sadowski, S.J., Ito, M., Bansal, A., Ky, B., Figueroa, D.J., Jiang, Q., Austin, C.P., MacNeil, D.J., Ishihara, A., Ihara, M., Kanatani, A., Van der Ploeg, L.H., Howard, A.D. & Liu, Q. (2001) Identification and characterization of a second melanin-concentrating hormone receptor, MCH-2R. Proc. Natl Acad. Sci. USA, 98, 7564-7569.
Saito, Y., Nothacker, H.P., Wang, Z., Lin, S.H., Leslie, F. & Civelli, O. (1999) Molecular characterization of the melanin-concentrating- hormone receptor. Nature, 400, 265-269.
Segal-Lieberman, G., Bradley, R.L., Kokkotou, E., Carlson, M., Trombly, D.J., Wang, X., Bates, S., Myers, M.G. Jr, Flier, J.S. & Maratos-Flier, E. (2003) Melanin-concentrating hormone is a critical mediator of the leptin-deficient phenotype. Proc. Natl Acad. Sci. USA, 100, 10085-10090.
Seutin, V., Scuvee-Moreau, J. & Dresse, A. (1997) Evidence for a non-GABAergic action of quaternary salts of bicuculline on dopaminergic neurones. Neuropharmacology, 36, 1653-1657.
Seutin, V., Scuvee-Moreau, J., Massotte, L. & Dresse, A. (1995) Hydrogen peroxide hyperpolarizes rat CA1 pyramidal neurons by inducing an increase in potassium conductance. Brain Res., 683, 275-278.
Shimada, M., Tritos, N.A., Lowell, B.B., Flier, J.S. & Maratos-Flier, E. (1998) Mice lacking melanin-concentrating hormone are hypophagic and lean. Nature, 396, 670-674.
Shimomura, Y., Mori, M., Sugo, T., Ishibashi, Y., Abe, M., Kurokawa, T., Onda, H., Nishimura, O., Sumino, Y. & Fujino, M. (1999) Isolation and identification of melanin-concentrating hormone as the endogenous ligand of the SLC-1 receptor. Biochem. Biophys. Res. Commun., 261, 622-626.
Tan, C.P., Sano, H., Iwaasa, H., Pan, J., Sailer, A.W., Hreniuk, D.L., Feighner, S.D., Palyha, O.C., Pong, S.S., Figueroa, D.J., Austin, C.P. & Jiang, M.M., Yu, H., Ito, J., Ito, M., Guan, X.M., MacNeil, D.J., Kanatani, A., Van der Ploeg, L.H. & Howard, A.D. (2002) Melanin-concentrating hormone receptor subtypes 1 and 2: species-specific gene expression. Genomics, 79, 785-792.
Toumaniantz, G., Bittencourt, J.C. & Nahon, J.L. (1996) The rat melanin-concentrating hormone gene encodes an additional putative protein in a different reading frame. Endocrinology, 137, 4518-4521.
Varas, M., Perez, M., Monzon, M.E. & de Barioglio, S.R. (2002) Melanin-concentrating hormone, hippocampal nitric oxide levels and memory retention. Peptides, 23, 2213-2221.
Varas, M.M., Perez, M.F., Ramirez, O.A. & de Barioglio, S.R. (2003) Increased susceptibility to LTP generation and changes in NMDA-MR1 and - NR2B subunits mRNA expression in rat hippocampus after MCH administration. Peptides, 24, 1403-1411.
Verlaet, M., Adamantidis, A., Coumans, B., Chanas, G., Zorzi, W., Meinen, E., Grisar, T. & Lakaye, B. (2002) Human immune cells express ppMCH mRNA and functional MCHR1 receptor. FEBS Lett., 527, 205-210.
Verret, L., Goutagny, R., Fort, P., Cagnon, L., Salvert, D., Leger, L., Boissard, R., Salin, P., Peyron, C. & Luppi, P.H. (2003) A role of melanin-concentrating hormone producing neurons in the central regulation of paradoxical sleep. BMC Neurosci., 4, 19.
Wang, S., Behan, J., O'Neill, K., Weig, B., Fried, S., Laz, T., Bayne, M., Gustafson, E. & Hawes, B.E. (2001) Identification and pharmacological characterization of a novel human melanin-concentrating hormone receptor, mch-r2. J. Biol. Chem., 276, 34664-34670.
Zhou, Q., Le Greves, P., Ragnar, F. & Nyberg, F. (2000) Intracerebroventricular injection of the N-terminal substance P fragment SP (1-7) regulates the expression of the N-methyl-D-aspartate receptor NR1, NR2A and NR2B subunit mRNAs in the rat brain. Neurosci. Lett., 291, 109-112.