Functional dissociation of group III metabotropic glutamate receptors revealed by direct comparison between the behavioral profiles of knockout mouse lines

International Journal of Neuropsychopharmacology

Volumn 18, Issue 11, 2015, Pages

  Goddyn, Hannelore ^a   Callaerts Vegh, Zsuzsanna ^a   D'Hooge, Rudi ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Behavioral phenotyping; Behavioral test battery; Knockout mice; Metabotropic glutamate receptors

Indexed keywords

METABOTROPIC RECEPTOR 4; METABOTROPIC RECEPTOR 7; METABOTROPIC RECEPTOR 8; METABOTROPIC RECEPTOR;

AMYGDALA; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BODY WEIGHT; BRAIN STEM; CEREBELLUM; COGNITION; COMPARATIVE STUDY; CONTROLLED STUDY; CORPUS STRIATUM; DENTATE GYRUS; EXPERIMENTAL BEHAVIORAL TEST; EXPLORATORY BEHAVIOR; FEAR; FEMALE; FUNCTIONAL DISSOCIATION; GENE DELETION; GENETIC BACKGROUND; GRIP STRENGTH; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; MEMORY; MOTIVATION; MOTONEURON; MOUSE; MULTIVARIATE ANALYSIS; NEOCORTEX; NONHUMAN; OLFACTORY BULB; PHENOTYPE; PREPULSE INHIBITION; PRIORITY JOURNAL; SPATIAL LEARNING; STARTLE REFLEX; THALAMUS; ANIMAL; C57BL MOUSE; DRUG EFFECTS; GENETICS; KNOCKOUT MOUSE; LEARNING; METABOLISM; MOTOR ACTIVITY; PHYSIOLOGY;

ANIMALS; BODY WEIGHT; EXPLORATORY BEHAVIOR; FEAR; FEMALE; LEARNING; MEMORY; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTIVATION; MOTOR ACTIVITY; MULTIVARIATE ANALYSIS; RECEPTORS, METABOTROPIC GLUTAMATE; REFLEX, STARTLE;

EID: 84984706137     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1093/ijnp/pyv053     Document Type: Article

References (66)

1. Bradley SR, Standaert DG, Rhodes, KJ, Rees HD, Testa CM, Levey AI, Conn PJ (1999) Immunohistochemical localization of subtype 4a metabotropic glutamate receptors in the rat and mouse basal ganglia. J Comp Neurol 407:33-46.
2. Caeyenberghs K, Balschun D, Roces DP, Schwake M, Saftig P, D'Hooge R (2006) Multivariate neurocognitive and emotional profle of a mannosidosis murine model for therapy assessment. Neurobiol Dis 23:422-432.
3. Callaerts-Vegh Z, Beckers T, Ball SM, Baeyens F, Callaerts PF, Cryan JF, Molnar E, D'Hooge R (2006) Concomitant defcits in working memory and fear extinction are functionally dissociated from reduced anxiety in metabotropic glutamate receptor 7-defcient mice. J Neurosci 26:6573-6582.
4. Corti C, Restituito S, Rimland JM, Brabet I, Corsi M, Pin JP, Fer-raguti F (1998) Cloning and characterization of alternative mRNA forms for the rat metabotropic glutamate receptors mGluR7 and mGluR8. Eur J Neurosci 10:3629-3641.
5. Corti C, Aldegheri L, Somogyi P, Ferraguti F (2002) Distribution and synaptic localisation of the metabotropic glutamate receptor 4 (mGluR4) in the rodent CNS. Neuroscience 110:403-420.
6. Crabbe JC, Wahlsten D, Dudek BC (1999) Genetics of mouse behavior: interactions with laboratory environment. Science 284:1670-1672.
7. Cryan JF, Kelly PH, Neijt HC, Sansig G, Flor PJ, van Der Putten H (2003) Antidepressant and anxiolytic-like effects in mice lacking the group III metabotropic glutamate receptor mGluR7. Eur J Neurosci 17:2409-2417.
8. - mice. Behav Brain Res 229:21-28.
9. Davis MJ, Duvoisin RM, Raber J (2013) Related functions of mGlu4 and mGlu8. Pharmacol Biochem Behav 111:11-16.
10. D'Hooge R, Deyn PP De (2001) Applications of the Morris water maze in the study of learning and memory. Brain Res Brain Res Rev 36:60-90.
11. Dobi A, Sartori SB, Busti D, Van der Putten H, Singewald N, Shi-gemoto R, Ferraguti F (2013) Neural substrates for the distinct effects of presynaptic group III metabotropic glutamate receptors on extinction of contextual fear conditioning in mice. Neuropharmacology 66:274-289.
12. Duvoisin R, Zhang C, Ramonell K (1995) A novel metabotropic glutamate receptor expressed in the retina and olfactory bulb. J Neurosci 15:3075-3083.
13. Duvoisin RM, Zhang C, Pfankuch TF, O'Connor H, Gayet-Primo J, Quraishi S, Raber J (2005) Increased measures of anxiety and weight gain in mice lacking the group III metabotropic gluta-mate receptor mGluR8. Eur J Neurosci 22:425-436.
14. Fendt M, Bürki H, Imobersteg S, van der Putten H, McAllister K, Leslie JC, Shaw D, Hölscher C (2010) The effect of mGlu8 def-ciency in animal models of psychiatric diseases. Genes Brain Behav 9:33-44.
15. Fendt M, Imobersteg S, Peterlik D, Chaperon F, Mattes C, Witt-mann C, Olpe H-R, Mosbacher J, Vranesic I, van der Putten H, McAllister KH, Flor PJ, Gee CE (2013) Differential roles of mGlu(7) and mGlu(8) in amygdala-dependent behavior and physiology. Neuropharmacology 72:215-223.
16. Ferraguti F, Klausberger T, Cobden P, Baude A, Roberts JDB, Szucs P, Kinoshita A, Shigemoto R, Somogyi P, Dalezios Y (2005). Metabotropic glutamate receptor 8-expressing nerve terminals target subsets of GABAergic neurons in the hippocampus. J Neurosci 25:10520-10536.
17. Gerlai R, Adams B, Fitch T, Chaney S, Baez M (2002) Performance defcits of mGluR8 knockout mice in learning tasks: the effects of null mutation and the background genotype. Neu-ropharmacology 43:235-249.
18. Goddyn H, Leo S, Meert T, D'Hooge R (2006) Differences in behavioral test battery performance between mice with hippocam-pal and cerebellar lesions. Behav Brain Res 173:138-147.
19. Goddyn H, Callaerts-Vegh Z, Stroobants S, Dirikx T, Vansteenwe-gen D, Hermans D, van der Putten H, D'Hooge R (2008) Def-cits in acquisition and extinction of conditioned responses in mGluR7 knockout mice. Neurobiol Learn Mem 90:103-111.
20. Iscru E, Goddyn H, Ahmed T, Callaerts-Vegh Z, D'Hooge R, Bals-chun D (2013) Improved spatial learning is associated with increased hippocampal but not prefrontal long-term potentia-tion in mGluR4 knockout mice. Genes, Brain Behav 12:615-625.
21. Kinoshita A, Ohishi H, Nomura S, Shigemoto R, Nakanishi S, Mizuno N (1996) Presynaptic localization of a metabotropic glutamate receptor, mGluR4a, in the cerebellar cortex: a light and electron microscope study in the rat. Neurosci Lett 207:199-202.
22. Kinoshita A, Shigemoto R, Ohishi H, van der Putten H, Mizuno N (1998) Immunohistochemical localization of metabotropic glutamate receptors, mGluR7a and mGluR7b, in the central nervous system of the adult rat and mouse: a light and electron microscopic study. J Comp Neurol 393:332-352.
23. Kinzie JM, Saugstad JA, Westbrook GL, Segerson TP (1995) Distribution of metabotropic glutamate receptor 7 messenger RNA in the developing and adult rat brain. Neurosci 69:167-176.
24. Kinzie JM, Shinohara MM, van den Pol AN, Westbrook GL, Seger-son TP (1997) Immunolocalization of metabotropic glutamate receptor 7 in the rat olfactory bulb. J Comp Neurol 385:372-384.
25. Kosinski CM, Bradley SR, Conn PJ, Levey AI, Landwehrmeyer GB, Penney Jr. JB, Young AB, Standaert DG (1999) Localization of metabotropic glutamate receptor 7 mRNA and mGluR7a protein in the rat basal ganglia. J Comp Neurol 415:266-284.
26. Kuramoto E, Fujiyama F, Unzai T, Nakamura K, Hioki H, Furuta T, Shigemoto R, Ferraguti F, Kaneko T (2007) Metabotropic gluta-mate receptor 4-immunopositive terminals of medium-sized spiny neurons selectively form synapses with cholinergic interneurons in the rat neostriatum. J Comp Neurol 500:908-922.
27. Leighty RE, Nilsson LNG, Potter H, Costa DA, Low MA, Bales KR, Paul SM, Arendash GW (2004) Use of multimetric statistical analysis to characterize and discriminate between the performance of four Alzheimer's transgenic mouse lines differing in Abeta deposition. Behav Brain Res 153:107-121.
28. Linden A-M, Johnson B, Peters S, Shannon H, Tian M, Wang Y, Yu J, Köster A, Baez M, Schoepp D. (2002) Increased anxiety-related behavior in mice defcient for metabotropic glutamate 8 (mGlu8) receptor. Neuropharmacology 43:251-259.
29. Lubbers ME, van den Bos R, Spruijt BM (2007) Mu opioid receptor knockout mice in the Morris Water Maze: a learning or motivation defcit? Behav Brain Res 180:107-111.
30. Masugi M, Yokoi M, Shigemoto R, Muguruma K, Watanabe Y, Sansig G, van der Putten H, Nakanishi S (1999) Metabotropic glutamate receptor subtype 7 ablation causes defcit in fear response and conditioned taste aversion. J Neurosci 19:955-963.
31. Mateos JM, Azkue J, Sarría R, Kuhn R, Grandes P, Knöpfel T (1998) Localization of the mGlu4a metabotropic glutamate receptor in rat cerebellar cortex. Histochem Cell Biol 109:135-139.
32. Messenger MJ, Dawson LG, Duty S (2002) Changes in metabo-tropic glutamate receptor 1-8 gene expression in the rodent basal ganglia motor loop following lesion of the nigrostriatal tract. Neuropharmacology 43:261-271.
33. Mineur YS, Crusio WE (2009) Behavioral effects of ventilated micro-environment housing in three inbred mouse strains. Physiol Behav 97:334-340.
34. Mogenson G, Jones D, Yim C (1980) From motivation to action: Functional interface between the limbic system and the motor system. Prog Neurobiol 14:69-97.
35. Nakajima Y, Iwakabe H, Akazawa C, Nawa H, Shigemoto R, Miz-uno N, Nakanishi S (1993) Molecular characterization of a novel retinal metabotropic glutamate receptor mGluR6 with a high agonist selectivity for L-2-amino-4-phosphonobu-tyrate. J Biol Chem 268:11868-11873.
36. Niswender CM, Conn PJ (2010) Metabotropic glutamate receptors: physiology, pharmacology, and disease. Annu Rev Pharmacol Toxicol 50:295-322.
37. O'Connor RM, Thakker DR, Schmutz M, van der Putten H, Hoyer D, Flor PJ, Cryan JF (2013) Adult siRNA-induced knockdown of mGlu7 receptors reduces anxiety in the mouse. Neurophar-macology 72:66-73.
38. Ohishi H, Akazawa C, Shigemoto R, Nakanishi S, Mizuno N (1995) Distributions of the mRNAs for L-2-amino-4-phosphonobu-tyrate-sensitive metabotropic glutamate receptors, mGluR4 and mGluR7, in the rat brain. J Comp Neurol 360:555-570.
39. Okamoto N, Hori S, Akazawa C, Hayashi Y, Shigemoto R, Mizuno N, Nakanishi S (1994) Molecular characterization of a new metabotropic glutamate receptor mGluR7 coupled to inhibitory cyclic AMP signal transduction. J Biol Chem 269:1231-1236.
40. Palazzo E, Marabese I, Soukupova M, Luongo L, Boccella S, Giordano C, de Novellis V, Rossi F, Maione S (2011) Metabo-tropic glutamate receptor subtype 8 in the amygdala modulates thermal threshold, neurotransmitter release, and rostral ventromedial medulla cell activity in infammatory pain. J Neurosci 31:4687-4697.
41. Palucha A, Klak K, Branski P, van der Putten H, Flor PJ, Pilc A (2007) Activation of the mGlu7 receptor elicits antidepressant-like effects in mice. Psychopharmacology (Berl) 194:555-562.
42. Pamidimukkala J, Hoang CJ, Hay M (2002) Expression of metabo-tropic glutamate receptor 8 in autonomic cell groups of the medulla oblongata of the rat. Brain Res 957:162-173.
43. Paradee W, Melikian HE, Rasmussen DL, Kenneson A, Conn PJ, Warren ST (1999) Fragile X mouse: strain effects of knockout phenotype and evidence suggesting defcient amygdala function. Neuroscience 94:185-192.
44. Paylor R, Crawley JN (1997) Inbred strain differences in prepulse inhibition of the mouse startle response. Psychopharmacol-ogy (Berl) 132:169-180.
45. Pekhletski R, Gerlai R, Overstreet LS, Huang X-P, Agopyan N, Slater NT, Abramow-Newerly W, Roder JC, Hampson DR (1996) Impaired cerebellar synaptic plasticity and motor performance in mice lacking the mGluR4 subtype of metabotropic glutamate receptor. J Neurosci 16:6364-6373.
46. Phillips T, Makoff A, Brown S, Rees S, Emson P (1997) Localization of mGluR4 protein in the rat cerebral cortex and hippocampus. Neuroreport 8:3349-3354.
47. Pin J-PP, Duvoisin R (1995) The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34:1-26.
48. Raber J, Duvoisin RM (2015). Novel metabotropic glutamate receptor 4 and glutamate receptor 8 therapeutics for the treatment of anxiety. Expert Opin Investig Drugs, 24:519-528.
49. Récasens M, Guiramand J, Aimar R, Abdulkarim A, Barbanel G (2007) Metabotropic glutamate receptors as drug targets. Curr Drug Targets 8:651-681.
50. Robbins MJ, Starr KR, Honey A, Soffn EM, Rourke C, Jones GA, Kelly FM, Strum J, Melarange RA, Harris AJ, Rocheville M, Rup-niak T, Murdock PR, Jones DNC, Kew JNC, Maycox PR (2007) Evaluation of the mGlu8 receptor as a putative therapeutic target in schizophrenia. Brain Res 1152:215-227.
51. Robbins TW, Everitt BJ (1996) Neurobehavioral mechanisms of reward and motivation. Curr Opin Neurobiol 6:228-236.
52. Saugstad JA, Kinzie JM, Shinohara MM, Segerson TP, Westbrook GL (1997) Cloning and expression of rat metabotropic gluta-mate receptor 8 reveals a distinct pharmacological profle. Mol Pharmacol 51:119-125.
53. Schoepp DD (2001) Unveiling the functions of presynaptic metabotropic glutamate receptors in the central nervous system. J Pharmacol Exp Ther 299:12-20.
54. Shigemoto R, Kinoshita A, Wada E, Nomura S, Ohishi H, Takada M, Flor PJ, Neki A, Abe T, Nakanishi S, Mizuno N (1997) Differential presynaptic localization of metabotropic gluta-mate receptor subtypes in the rat hippocampus. J Neurosci 17:7503-7522.
55. Shoemaker JM, Saint Marie RL, Bongiovanni MJ, Neary AC, Tochen LS, Swerdlow NR (2005) Prefrontal D1 and ventral hip-pocampal N-methyl-D-aspartate regulation of startle gating in rats. Neuroscience 135:385-394.
56. Somogyi P, Dalezios Y, Luján R, Roberts JDB, Watanabe M, Shige-moto R (2003) High level of mGluR7 in the presynaptic active zones of select populations of GABAergic terminals innervating interneurons in the rat hippocampus. Eur J Neurosci 17:2503-2520.
57. Swanson CJ, Bures M, Johnson MP, Linden A-M, Monn J a, Sch-oepp DD (2005) Metabotropic glutamate receptors as novel targets for anxiety and stress disorders. Nat Rev Drug Discov 4:131-144.
58. Swerdlow NR, Paulsen J, Braff DL, Butters N, Geyer MA, Swenson MR (1995) Impaired prepulse inhibition of acoustic and tactile startle response in patients with Huntington's disease. J Neu-rol Neurosurg Psychiatry 58:192-200.
59. Swerdlow NR, Braff DL, Geyer M a (2000) Animal models of def-cient sensorimotor gating: what we know, what we think we know, and what we hope to know soon. Behav Pharmacol 11:185-204.
60. Swerdlow NR, Weber M, Qu Y, Light GA, Braff DL (2008) Realistic expectations of prepulse inhibition in translational models for schizophrenia research. Psychopharmacology (Berl) 199:331-388
61. Tanabe Y, Nomura A, Masu M, Shigemoto R, Mizuno N, Nakani-shi S (1993) Signal transduction, pharmacological properties, and expression patterns of two rat metabotropic glutamate receptors, mGluR3 and mGluR4. J Neurosci 13:1372-1378.
62. Testa CM, Standaert DG, Young AB, Penney JB Jr (1994) Metabo-tropic glutamate receptor mRNA expression in the basal ganglia of the rat. J Neurosci 14:3005-3018.
63. Wada E, Shigemoto R, Kinoshita A, Ohishi H, Mizuno N (1998) Metabotropic glutamate receptor subtypes in axon terminals of projection fbers from the main and accessory olfactory bulbs: a light and electron microscopic immunohistochemi-cal study in the rat. J Comp Neurol 393: 493-504.
64. Weber M, Schnitzler H-U, Schmid S (2002) Synaptic plasticity in the acoustic startle pathway: the neuronal basis for short-term habituation? Eur J Neurosci 16:1325-1332.
65. Wu S, Wright R a., Rockey PK, Burgett SG, Arnold JS, Rosteck PR, Johnson BG, Schoepp DD, Belagaje RM (1998) Group III human metabotropic glutamate receptors 4, 7 and 8: Molecular cloning, functional expression, and comparison of pharmacological properties in RGT cells. Mol Brain Res 53:88-97.
66. Zhang W (2001) The ventral hippocampus and fear conditioning in rats: different anterograde amnesias of fear after infusion of N-methyl-?-aspartate or its noncompetitive antagonist MK-801 into the ventral hippocampus. Behav Brain Res 126:159-174.