Presynaptic release-regulating mGlu1 receptors in central nervous system

Frontiers in Pharmacology

Volumn 7, Issue AUG, 2016, Pages

  Pittaluga, Anna ^a,b  

^a UNIVERSITY OF GENOA   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

Author keywords

Autoreceptors; Heteroreceptors; mGlu1 receptors; Presynaptic receptors; Transmitter release

Indexed keywords

G PROTEIN COUPLED RECEPTOR; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR 5; METABOTROPIC RECEPTOR AGONIST; METABOTROPIC RECEPTOR ANTAGONIST;

BINDING AFFINITY; BINDING SITE; CENTRAL NERVOUS SYSTEM; CHROMATIN IMMUNOPRECIPITATION; EXOCYTOSIS; GENE EXPRESSION PROFILING; HUMAN; IMMUNOREACTIVITY; IN VITRO STUDY; MEMBRANE DEPOLARIZATION; NERVE ENDING; NEUROTRANSMISSION; NONHUMAN; PRESYNAPTIC POTENTIAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; REVIEW; SIGNAL TRANSDUCTION; SYNAPTOSOME; THERMOSTABILITY;

EID: 84988735035     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2016.00295     Document Type: Review

References (92)

1. Aiba, A., Chen, C., Herrup, K., Rosenmund, C., Stevens, C. F., and Tonegawa, S. (1994). Reduced hippocampal long-term potentiation and context-specific deficit in associative learning in mGlur1 mutant mice. Cell 79, 365-375. doi: 10.1016/0092-8674(94)90204-6
2. Battaglia, G., Bruno, V., Pisani, A., Centonze, D., Catania, M. V., Calabresi, P., et al. (2001). Selective blockade of type-1 metabotropic glutamate receptors induces neuroprotection by enhancing GABAergic transmission. Mol. Cell. Neurosci. 17, 1071-1083. doi: 10.1006/mcne.2001.0992
3. Benquet, P., Gee, C. E., and Gerber, U. (2002). Two distinct signaling pathways upregulate NMDA receptor responses via two distinct metabotropic glutamate receptor subtypes. J. Neurosci. 22, 9679-9686. doi: 10.1016/j.neuropharm.2008.05.020
4. Bonsi, P., Platania, P., Martella, G., Madeo, G., Vita, G., Tassone, A., et al. (2008). Distinct role of group I mGlu receptors in striatal functions. Neuropharmacology 55, 392-395. doi: 10.1016/j.neuropharm.2008.05.020
5. Bordi, F., and Ugolini, A. (1999). Group I metabotropic glutamate receptors: implications for brain diseases. Prog. Neurobiol. 59, 55-79. doi: 10.1016/S0301-0082(98)00095-1
6. Bruno, V., Battaglia, G., Copani, A., Cespedes, V. M., Galindo, M. F., Cena, V., et al. (2001). An activity-dependent switch from facilitation to inhibition in the control of excitotoxicity by group I metabotropic glutamate receptors. Eur. J. Neurosci. 13, 1469-1478. doi: 10.1046/j.0953-816x.2001.01541.x
7. Cartmell, J., and Schoepp, D. D. (2000). Regulation of transmitter release by metabotropic glutamate receptors. J. Neurochem. 75, 889-907. doi: 10.1046/j.1471-4159.2000.0750889.x
8. Cervetto, C., Maura, G., and Marcoli, M. (2010). Inhibition of presynaptic release-facilitatory kainate autoreceptors by extracellular cyclic GMP. J. Pharmacol. Exp. Ther. 332, 210-219. doi: 10.1124/jpet.109.154955
9. Coffey, E. T., Herrero, I., Sihra, T. S., Sánchez-Prieto, J., and Nicholls, D. G. (1994). Glutamate exocytosis and MARCKS phosphorylation are enhanced by a metabotropic glutamate receptor coupled to protein kinase C synergistically activated by diacylglycerol and arachidonic acid. J. Neurochem. 63, 1303-1310. doi: 10.1046/j.1471-4159.1994.63041303.x
10. Conn, P. J., Battaglia, G., Marino, M. J., and Nicoletti, F. (2005). Metabotropic glutamate receptors in basal ganglia motor circuit. Nature Rev. Neurosci. 6, 787-798. doi: 10.1038/nrn1763
11. Conquet, F., Bashir, Z. I., Davies, C. H., Daniel, H., Ferraguti, F., Bordi, F., et al. (1994). Motor deficit and impairment of synaptic plasticity in mice lacking mGluR1. Nature 372, 237-243. doi: 10.1038/372237a0
12. Conti, V., Aghaie, A., Cilli, M., Martin, N., Caridi, G., Musante, L., et al. (2006). crv4, a mouse model for human ataxia associated with kyphoscoliosis caused by an mRNA splicing mutation of the metabotropic glutamate receptor 1 (Grm1). Int. J. Mol. Med. 18, 593-600. doi: 10.3892/ijmm.18.4.593
13. Croucher, M. J., Thomas, L. S., Ahmadi, H., Lawrence, V., and Harris, J. R. (2001). Endogenous sulphur-containing amino acids: potent agonists at presynaptic metabotropic glutamate autoreceptors in the rat central nervous system. Br. J. Pharmacol. 133, 815-824. doi: 10.1038/sj.bjp.0704138
14. De Blasi, A., Conn, P. J., Pin, J., and Nicoletti, F. (2001). Molecular determinants of metabotropic glutamate receptor signaling. Trends Pharmacol. Sci. 22, 114-120. doi: 10.1016/S0165-6147(00)01635-7
15. De Novellis, V., Marabese, I., Uliano, R., Palazzo, E., Scafuro, A., Rossi, F., et al. (2002). Type I and II metabotropic glutamate receptors modulate periaqueductal grey glycine release: interaction between mGlu2/3 and A1 adenosine receptors. Neuropharmacology 43, 1061-1069. doi: 10.1016/S0028-3908(02)00227-7
16. Delille, H. K., Becker, J. M., Burkhardt, S., Bleher, B., Terstappen, G. C., Schmidt, M., et al. (2012). Heterocomplex formation of 5-HT2A-mGlu2 and its relevance for cellular signaling cascades. Neuropharmacology 62, 2184-2191. doi: 10.1016/j.neuropharm.2012.01.010
17. Di Prisco, S., Merega, E., Bonfiglio, T., Olivero, G., Cervetto, C., Grilli, M., et al. (2016). Presynaptic, release-regulating mGlu2-preferring and mGlu3-preferring autoreceptors in CNS: pharmacological profiles and functional roles in demyelinating disease. Br. J. Pharmacol. 173, 1465-1477. doi: 10.1111/bph.13442
18. Doumazane, E., Scholler, P., Zwier, J. M., Trinquet, E., Rondard, P., and Pin, J. P. (2010). A new approach to analyze cell surface protein complexes reveals specific heterodimeric metabotropic glutamate receptors. FASEB J. 25, 66-77. doi: 10.1096/fj.10-163147
19. Dunkley, P. R., Jarvie, P. E., Heath, J. W., Kiddn, G. J., and Rostas, J. A. P. (1986). A rapid method for isolation of synaptosomes on Percoll gradient. Brain Res. 372, 115-129. doi: 10.1016/0006-8993(86)91464-2
20. Fazal, A., Parker, F., Palmer, A. M., and Croucher, M. J. (2003). Characterisation of the actions of group i metabotropic glutamate receptor subtype selective ligands on excitatory amino acid release and sodium-dependent re-uptake in rat cerebrocortical mini slices. J. Neurochem. 86, 1346-1358. doi: 10.1046/j.1471-4159.2003.01932.x
21. Feligioni, M., Raiteri, L., Pattarini, R., Grilli, M., Bruzzone, S., Cavazzani, P., et al. (2003). The Human immuodeficiency virus-1 protein tat and its discrete fragments evoke selective release of acetylcholine from human and rat cerebrocortical terminals through species-specific mechanisms. J. Neurosci. 23, 6810-6818.
22. Ferraguti, F., Crepaldi, L., and Nicoletti, F. (2008). Metabotropic glutamate 1 receptor: current concepts and perspectives. Pharmacol. Rev. 60, 536-581. doi: 10.1124/pr.108.000166
23. Fink, K., Bönisch, H., and Göthert, M. (1989). Presynaptic NMDA receptors stimulate noradrenaline release in the cerebral cortex. Eur. J. Pharmacol. 185, 115-117. doi: 10.1016/0014-2999(90)90219-V
24. Fotuhi, M., Sharp, A. H., Glatt, C. E., Hwang, P. M., Vonkrosigk, M., Snyder, S. H., et al. (1993). Differential localization of phosphoinositide-linked metabotropic glutamate receptor (mGluR1) and the inositol 1,4,5-trisphosphate receptor in rat brain. J. Neurosci. 13, 2001-2012.
25. Gemignani, A., Paudice, P., Pittaluga, A., and Raiteri, M. (2000). The HIV-1 coat protein gp120 and some of its fragments potently activate native cerebral NMDA receptors mediating neuropeptide release. Eur. J. Neurosci. 12, 2839-2846. doi: 10.1046/j.1460-9568.2000.00172.x
26. Gereau, R. W., and Conn, P. J. (1995). Multiple presynaptic metabotropic glutamate receptors modulate excitatory and inhibitory synaptic transmission in hippocampal area CA1. J. Neurosci. 15, 6879-6889.
27. Giribaldi, F., Milanese, M., Bonifacino, T., Rossi, P. I. A., Di Prisco, S., Pittaluga, A., et al. (2013). Group I metabotropic glutamate autoreceptors induce abnormal glutamate exocytosis in a mouse model of amyotrophic lateral sclerosis. Neuropharmacology 66, 253-263. doi: 10.1016/j.neuropharm.2012.05.018
28. Grilli, M., Summa, M., Salmone, A., Olivero, G., Zappettini, S., Di Prisco, S., et al. (2012). In vitro exposure to nicotine induces endocytosis of presynaptic AMPA receptors modulating dopamine release in rat nucleus accumbens nerve terminals. Neuropharmacology 63, 916-926. doi: 10.1016/j.neuropharm.2012.06.049
29. Grilli, M., Zappettini, S., Zanardi, A., Lagomarsino, F., Pittaluga, A., Zoli, M., et al. (2009). Exposure to an enriched environment selectively increases the functional response of the pre-synaptic NMDA receptors which modulate noradrenaline release in mouse hippocampus. J. Neurochem. 110, 1598-1606. doi: 10.1111/j.1471-4159.2009.06265.x
30. Herrero, I., Miras-Portugal, M. T., and Sanchez-Prieto, J. (1992). Positive feedback of glutamate exocytosis by metabotropic presynaptic receptor stimulation. Nature 360, 163-166. doi: 10.1038/360163a0
31. Herrero, I., Miras-Portugal, M. T., and Sanchez-Prieto, J. (1994). Rapid desensitization of the presynaptic metabotropic receptor that facilitates glutamate exocytosis. Eur. J. Neurosci. 6, 115-120. doi: 10.1111/j.1460-9568.1994.tb00253.x
32. Herrero, I., Miras-Portugal, M. T., and Sanchez-Prieto, J. (1998). Functional switch from facilitation to inhibition in the control of glutamate release by metabotropic glutamate receptors. J. Biol. Chem. 273, 1951-1958. doi: 10.1074/jbc.273.4.1951
33. Hsia, A. Y., Salin, P. A., Castillo, P. E., Aiba, A., Abeliovich, A., Tonegawa, S., et al. (1995). Evidence against a role for metabotropic glutamate receptors in mossy fibre LTP: the use of mutant mice and pharmacological antagonists. Neuropharmacology 34, 1567-1572. doi: 10.1016/0028-3908(95)00115-M
34. Hu, H. J., Alter, B. J., Carrasquillo, Y., Qiu, C. S., and Gereau, R. W. IV (2007). Metabotropic glutamate receptor 5 modulates nociceptive plasticity via extracellular signal-regulated kinase-Kv4.2 signaling in spinal cord dorsal horn neurons. J. Neurosci. 27, 13181-13191. doi: 10.1523/JNEUROSCI.0269-07.2007
35. Hu, H. J., and Gereau, R. W. IV (2011). Metabotropic glutamate receptor 5 regulates excitability and Kv4.2-containing K+ channels primarily in excitatory neurons of the spinal dorsal horn. J. Neurophysiol. 105, 3010-3021. doi: 10.1152/jn.01050.2010
36. Hubert, G. W., Paquet, M., and Smith, Y. (2001). Differential subcellular localization of mGluR1a and mGluR5 in the rat and monkey substantia nigra. J. Neurosci. 21, 1838-1847.
37. Ito, M. (2002). The molecular organization of cerebellar long-term depression. Nat. Rev. Neurosci. 3, 896-902. doi: 10.1038/nrn962
38. Ito, M., and Kano, M. (1982). Long-lasting depression of parallel fibre-Purkinje cell transmission induced by conjunctive stimulation of parallel fibres and climbing fibres in the cerebellar cortex. Neurosci. Lett. 33, 253-258. doi: 10.1016/0304-3940(82)90380-9
39. Lefebvre, C., Fisher, K., Cahill, C. M., and Coderre, T. J. (2000). Evidence that DHPG-induced nociception depends on glutamate release from primary afferent C-fibres. Neuroreport 11, 1631-1635. doi: 10.1097/00001756-200006050-00007
40. Linden, D. J., and Connor, J. A. (1993). Cellular mechanisms of long-term depression in the cerebellum. Curr. Opin. Neurobiol. 3, 401-406. doi: 10.1016/0959-4388(93)90133-J
41. Longordo, F., Feligioni, M., Chiaramonte, G., Sbaffi, P. F., Raiteri, M., and Pittaluga, A. (2006). The human immunodeficiency virus-1 protein transactivator of transcription up-regulates N-methyl-D-aspartate receptor function by acting at metabotropic glutamate receptor 1 receptors coexisting on human and rat brain noradrenergic neurons. J. Pharmacol. Exp. Ther. 317, 1097-1105. doi: 10.1124/jpet.105.099630
42. Lorrain, D. S., Correa, L., Anderson, J., and Varney, M. (2002). Activation of spinal cord group I metabotropic glutamate receptors in rats evokes local glutamate release and spontaneous nociceptive behaviours: effect of 2-methyl-6-(phenylethynyl)-pyridine pretreatment. Neurosci. Lett. 327, 198-202. doi: 10.1016/S0304-3940(02)00393-2
43. Lu, Y., Jia, Z., Janus, C., Henderson, J. T., Gerlai, R., Wojtowicz, J. M., et al. (1997). Mice lacking metabotropic glutamate receptor 5 show impaired learning and reduced CA1 long-term potentiation (LTP) but normal CA3 LTP. J. Neurosci. 17, 5196-5205.
44. Luccini, E., Musante, V., Neri, E., Brambilla Bas, M., Severi, P., Raiteri, M., et al. (2007a). Functional interactions between presynaptic NMDA receptors and metabotropic glutamate receptors co-expressed on rat and human noradrenergic terminals. Br. J. Pharmacol. 151, 1087-1094. doi: 10.1038/sj.bjp.0707280
45. Luccini, E., Musante, V., Neri, E., Raiteri, M., and Pittaluga, A. (2007b). N-methyl-D-aspartate autoreceptors respond to low and high agonist concentrations by facilitating, respectively, exocytosis and carrier-mediated release of glutamate in rat hippocampus. J. Neurosci. Res. 85, 3657-3665. doi: 10.1002/jnr.21446
46. Lujan, R., Nusser, Z., Roberts, J. D., Shigemoto, R., and Somogyi, P. (1996). Perysinaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus. Eur. J. Neurosci. 8, 1488-1500. doi: 10.1111/j.1460-9568.1996.tb01611.x
47. Mannaioni, G., Attucci, S., Missanelli, A., Pellicciari, R., Corradetti, R., and Moroni, F. (1999). Biochemical and electrophysiological studies on (S)-(+)-2-(3'-carboxybicyclo (1.1.1)pentyl)-glycine (CBPG), a novel mGlu5 receptor agonist endowed with mGlu1 receptor antagonist activity. Neuropharmacology 38, 917-926. doi: 10.1016/S0028-3908(99)00021-0
48. Mannaioni, G., Marino, M. J., Valenti, O., Traynelis, S. F., and Conn, P. J. (2001). Metabotropic glutamate receptors 1 and 5 differentially regulate CA1 pyramidal cell function. J. Neurosci. 21, 5925-5934.
49. Manzoni, O., and Bockaert, J. (1995). Metabotropic glutamate receptors inhibiting excitatory synapses in the CA1 area of rat hippocampus. Eur. J. Neurosci. 7, 2518-2523. doi: 10.1111/j.1460-9568.1995.tb01051.x
50. Marchi, M., and Grilli, M. (2010). Presynaptic nicotinic receptors modulating transmitter release in the central nervous system: functional interactions with other coexisting receptors. Prog. Neurobiol. 92, 105-111. doi: 10.1016/j.pneurobio.2010.06.004
51. Marchi, M., Grilli, M., and Pittaluga, A. (2015). Nicotinic modulation of glutamate receptor function at nerve terminal level: a fine-tuning of synaptic signals. Front. Pharmacol. 6:89. doi: 10.3389/fphar.2015.00089
52. Marchi, M., Pittaluga, A., and Grilli, M. (2014). A new specific neuronal modulatory effect of nicotine: the functional cross-talk between nicotinic and glutamate receptors. Rec. Clin. Inv. 1:e84.
53. Mateos, J. M., Benitez, R., Elezgarai, I., Azkue, J. J., Lazaro, E., Osorio, A., et al. (2000). Immunolocalization of the mGluR1b splice variant of the metabotropic glutamate receptor 1 at parallel fibre-Purkinje cells synapses in the rat cerebellar cortex. J. Neurochem. 74, 1301-1309. doi: 10.1046/j.1471-4159.2000.741301.x
54. Milanese, M., Bonifacino, T., Zappettini, S., Usai, C., Tacchetti, C., Nobile, M., et al. (2009). Glutamate release from astrocytic gliosomes under physiological and pathological conditions. Int. Rev. Neurobiol. 85, 295-318. doi: 10.1016/S0074-7742(09)85021-6
55. Milanese, M., Zappettini, S., Jacchetti, E., Bonifacino, T., Cervetto, C., Usai, C., et al. (2010). In vitro activation of GAT1 transporters expressed in spinal cord gliosomes stimulates glutamate release that is abnormally elevated in the SOD1/G93A(+) mouse model of amyotrophic lateral sclerosis. J. Neurochem. 113, 489-501. doi: 10.1111/j.1471-4159.2010.06628.x
56. Mills, C. D., Xu, G. Y., McAdoo, D. J., and Hulsebosh, C. E. (2001). Involvement of metabotropic glutamate receptors in excitatory aminoacid and GABA release following spinal cord injury in rat. J. Neurochem. 79, 835-848. doi: 10.1046/j.1471-4159.2001.00630.x
57. Moroni, F., Cozzi, A., Lombardi, G., Sourtcheva, S., Leonardi, P., Carfi, M., et al. (1998). Presynaptic mGlu1 type receptors potentiate transmitter output in the rat cortex. Eur. J. Pharmacol. 347, 189-195. doi: 10.1016/S0014-2999(98)00124-1
58. Muly, E. C., Maddox, M., and Smith, Y. (2003). Distribution of mGluR1 and mGluR5 immunolabelling in primate prefrontal cortex. J. Comp. Neurol. 467, 521-535. doi: 10.1002/cne.10937
59. Mura, E., Preda, S., Govoni, S., Lanni, C., Trabace, L., Grilli, M., et al. (2010). Specific neuromodulatory actions of amyloid-beta on dopamine release in rat nucleus accumbens and caudate putamen. J. Alzheimers Dis. 19, 1041-1053. doi: 10.3233/JAD-2010-1299
60. Musante, V., Longordo, F., Neri, E., Pedrazzi, M., Kalfas, F., Severi, P., et al. (2008a). RANTES modulates the release of glutamate in human neocortex. J. Neurosci. 28, 12231-12240. doi: 10.1523/JNEUROSCI.3212-08.2008
61. Musante, V., Neri, E., Feligioni, M., Puliti, A., Pedrazzi, M., Conti, V., et al. (2008b). Presynaptic mGlu1 and mGlu5 autoreceptors facilitate glutamate exocytosis from mouse cortical nerve endings. Neuropharmacology 55, 474-482. doi: 10.1016/j.neuropharm.2008.06.056
62. Musante, V., Summa, M., Cunha, R. A., Raiteri, M., and Pittaluga, A. (2011). Pre-synaptic glycine GlyT1 transporter-NMDA receptor interaction: relevance to NMDA autoreceptor activation in the presence of Mg2+ ions. J. Neurochem. 117, 516-527. doi: 10.1111/j.1471-4159.2011.07223.x
63. Musante, V., Summa, M., Neri, E., Puliti, A., Godowicz, T. T., Severi, P., et al. (2010). The HIV-1 viral protein Tat increases glutamate and decreases GABA exocytosis from human and mouse neocortical nerve endings. Cereb. Cortex 20, 1974-1984. doi: 10.1093/cercor/bhp274
64. Neri, E., Musante, V., and Pittaluga, A. (2007). Effects of the HIV-1 viral protein TAT on central neurotransmission: role of group I metabotropic glutamate receptors. Int. Rev. Neurobiol. 82, 339-356. doi: 10.1016/S0074-7742(07)82018-6
65. Nicoletti, F., Bockaert, J., Collingridge, G. L., Conn, P. J., Ferraguti, F., Schoepp, D. D., et al. (2011). Metabotropic glutamate receptors: from the workbench to the bedside. Neuropharmacology 60, 1017-1041. doi: 10.1016/j.neuropharm.2010.10.022
66. Nicoletti, F., Bruno, V., Catania, M. V., Battaglia, G., Copani, A., Barbagallo, G., et al. (1999). Group I metabotropic glutamate receptors: hypothesis to explain their dual role in neurotoxicity and neuroprotection. Neuropharmacology 38, 1477-1484. doi: 10.1016/S0028-3908(99)00102-1
67. Nicoletti, F., Bruno, V., Ngomba, R. T., Gradini, R., and Battaglia, G. (2015). Metabotropic glutamate receptors as drug targets: what's new? Curr. Opin. Pharmacol. 20, 89-94. doi: 10.1016/j.coph.2014.12.002
68. Nusser, Z., Mulvihill, E., Streit, P., and Somogy, P. (1994). Subsynaptic segregation of metabotropic and ionotropic glutamate receptors as revealed by immunogold localization. Neuroscience 61, 421-427. doi: 10.1016/0306-4522(94)90421-9
69. Parodi, M., Patti, L., Grilli, M., Raiteri, M., and Marchi, M. (2006). Nicotine has a permissive role on the activation of metabotropic glutamate 5 receptors coexisting with nicotinic receptors on rat hippocampal noradrenergic nerve terminals. Neurochem. Int. 48, 138-143. doi: 10.1016/j.neuint.2005.08.010
70. Pellegrini-Giampietro, D. E. (2003). The distinct role of mGlu1 receptors in post-ischemic neuronal death. Trends Pharmacol. Sci. 24, 461-470. doi: 10.1016/S0165-6147(03)00231-1
71. Pin, J.-P., and Bockaert, J. (1995). Get receptive to metabotropic glutamate receptors. Curr. Opin. Neurobiol. 5, 342-349. doi: 10.1016/0959-4388(95)80047-6
72. Pittaluga, A., Bonfanti, A., and Raiteri, M. (1997). Differential desensitization of ionotropic non-NMDA receptors having distinct neuronal location and function. Naunyn-Schmiedeb. Arch. Pharmacol. 356, 29-38. doi: 10.1007/PL00005025
73. Pittaluga, A., Feligioni, M., Longordo, F., Luccini, E., and Raiteri, M. (2006). Trafficking of presynaptic AMPA receptors mediating transmitter release: neuronal selectivity and relationships with sensitivity to cyclothiazide. Neuropharmacology 50, 286-296. doi: 10.1016/j.neuropharm.2005.09.004
74. Pittaluga, A., Pattarini, R., Feligioni, M., and Raiteri, M. (2001). NMDA receptors mediating hippocampal noradrenaline and striatal dopamine release display differential sensitivity to quinolinic acid, the HIV-1 envelope protein gp120, external pH and PKC inhibition. J. Neurochem. 76, 139-148. doi: 10.1046/j.1471-4159.2001.00057.x
75. Pittaluga, A., and Raiteri, M. (1990). Release-enhancing glycine-dependent presynaptic NMDA receptors exist on noradrenergic terminals of hippocampus. Eur. J. Pharmacol. 191, 231-234. doi: 10.1016/0014-2999(90)94153-O
76. Pittaluga, A., Segantini, D., Feligioni, M., and Raiteri, M. (2005). Extracellular protons differentially potentiate the responses of native AMPA receptor subtypes regulating transmitter release. Br. J. Pharmacol. 144, 293-299. doi: 10.1038/sj.bjp.0705960
77. Raiteri, L., and Raiteri, M. (2000). Synaptosomes still viable after 25 years of superfusion. Neurochem. Res. 25, 1265-1274. doi: 10.1023/A:1007648229795
78. Raiteri, M., Angelini, F., and Levi, G. (1974). A simple apparatus for studying the release of transmitters from synaptosomes. Eur. J. Pharmacol. 25, 411-414. doi: 10.1016/0014-2999(74)90272-6
79. Reid, M. E., Toms, N. J., Bedingfield, J. S., and Roberts, P. J. (1999). Group I mGlu receptors potentiate synaptosomal [3H]glutamate release independently of exogenously applied arachidonic acid. Neuropharmacology 38, 477-485. doi: 10.1016/S0028-3908(98)00217-2
80. Rodriguez-Moreno, A., Sistiaga, A., Lerma, J., and Sanchez-Prieto, J. (1998). Switch from facilitation to inhibition of excitatory synaptic transmission by group I mGluR desensitization. Neuron 21, 1477-1486. doi: 10.1016/S0896-6273(00)80665-0
81. Romano, C., Sesma, M. A., McDonald, C. T., O'Malley, K., Van den Pol, A. N., and Olney, J. W. (1995). Distribution of metabotropic glutamate receptor mGluR5 immunoreactivity in rat brain. J. Comp. Neurol. 335, 455-469. doi: 10.1002/cne.903550310
82. Rossi, P. I. A., Musante, I., Summa, M., Pittaluga, A., Emionite, L., Ikehata, M., et al. (2013). Compensatory molecular and functional mechanisms in neuronal cells/nervous system of the Grm1crv4 mouse lacking the mGlu1 receptor, a model for motor coordination deficits. Cereb. Cortex 23, 2179-2189. doi: 10.1093/cercor/bhs200
83. Schoepp, D. D. (2001). Unveiling the functions of presynaptic metabotropic glutamate receptors in the central nervous system. J. Pharmacol. Exp. Ther. 299, 12-20.
84. Shigemoto, R., Nomura, S., Ohishi, H., Nakanishi, S., and Mizuno, N. (1993). Immunohistochemical localization of a metabotropic glutamate receptor, mGluR5, in the rat brain. Neurosci. Lett. 163, 53-57. doi: 10.1016/0304-3940(93)90227-C
85. Sistiaga, A., Herrero, I., Conquet, F., and Sanchez-Prieto, J. (1998). The metabotropic glutamate receptor 1 is not involved in the facilitation of glutamate release in cerebrocortical nerve terminals. Neuropharmacology 37, 1485-1492. doi: 10.1016/S0028-3908(98)00129-4
86. Smolders, I., Lindekens, H., Clinckers, R., Meurs, A., O'Neill, M. J., Lodge, D., et al. (2004). In vivo modulation of extracellular hippocampal glutamate and GABA levels and limbic seizures by group I and II metabotropic glutamate receptor ligands. J. Neurochem. 88, 1068-1077. doi: 10.1046/j.1471-4159.2003.02251.x
87. Spampinato, F. S., Molinaro, G., Merlo, S., Iacovelli, L., Caraci, F., Battaglia, G., et al. (2012). Estrogen receptors and type 1 metabotropic glutamate receptors are interdependent in protecting cortical neurones againsts b-amyloid toxicity. Mol. Pharmacol. 81, 12-20. doi: 10.1124/mol.111.074021
88. Thomas, L. S., Jane, D. E., Harris, J. R., and Croucher, M. J. (2000). Metabotropic glutamate autoreceptors of the mGlu(5) subtype positively modulate neuronal glutamate release in the rat forebrain in vitro. Neuropharmacology 39, 1554-1566. doi: 10.1016/S0028-3908(99)00223-3
89. Vazquez, E., Herrero, I., Miras-Portugal, M. T., and Sanchez-Prieto, J. (1994). Facilitation of glutamate release by metabotropic glutamate receptors in hippocampal nerve terminals. Neurosci. Res. Comm. 15, 187-194.
90. Vazquez, E., Herrero, I., Miras-Portugal, M. T., and Sanchez-Prieto, J. (1995). Developmental change from inhibition to facilitation in the presynaptic control of glutamate exocytosis by metabotropic glutamate receptors. Neuroscience 68, 117-124. doi: 10.1016/0306-4522(95)00121-X
91. Vizi, E. S., Fekete, A., Karoly, R., and Mike, A. (2010). Nonsynaptic receptors and transporters involved in brain functions and targets of drug treatment. Br. J. Pharmacol. 160, 785-809. doi: 10.1111/j.1476-5381.2009.00624.x
92. Zucchini, S., Pittaluga, A., Summa, M., Brocca-Cofano, E., Fabris, M., De Michele, R., et al. (2013). Seizure susceptibility in tat-transgenic mice: implications for the role of tat in human immunodeficiency virus type 1 associated encephalopathy. Neurobiol. Dis. 62, 354-359. doi: 10.1016/j.nbd.2013.02.004