Generic placeholder image

Current Neuropharmacology


ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Review Article

The Modulation of Pain by Metabotropic Glutamate Receptors 7 and 8 in the Dorsal Striatum

Author(s): Serena Boccella, Ida Marabese, Francesca Guida, Livio Luongo, Sabatino Maione and Enza Palazzo*

Volume 18, Issue 1, 2020

Page: [34 - 50] Pages: 17

DOI: 10.2174/1570159X17666190618121859

Price: $65


The dorsal striatum, apart from controlling voluntary movement, displays a recently demonstrated pain inhibition. It is connected to the descending pain modulatory system and in particular to the rostral ventromedial medulla through the medullary dorsal reticular nucleus. Diseases of the basal ganglia, such as Parkinson's disease, in addition to being characterized by motor disorders, are associated with pain and hyperactivation of the excitatory transmission. A way to counteract glutamatergic hyperactivation is through the activation of group III metabotropic glutamate receptors (mGluRs), which are located on presynaptic terminals inhibiting neurotransmitter release. So far the mGluRs of group III have been the least investigated, owing to a lack of selective tools. More recently, selective ligands for each mGluR of group III, in particular positive and negative allosteric modulators, have been developed and the role of each subtype is starting to emerge. The neuroprotective potential of group III mGluRs in pathological conditions, such as those characterized by elevate glutamate, has been recently shown. In the dorsal striatum, mGluR7 and mGluR8 are located at glutamatergic corticostriatal terminals and their stimulation inhibits pain in pathological conditions such as neuropathic pain. The two receptors in the dorsal striatum have instead a different role in pain control in normal conditions. This review will discuss recent results focusing on the contribution of mGluR7 and mGluR8 in the dorsal striatal control of pain. The role of mGluR4, whose antiparkinsonian activity is widely reported, will also be addressed.

Keywords: mGluR7, mGluR8, dorsal striatum, chronic pain, descending pain modulatory system, hyperglutamatergism.

Graphical Abstract
Albin, R.L.; Young, A.B.; Penney, J.B. The functional anatomy of basal ganglia disorders. Trends Neurosci., 1989, 12(10), 366-375.
[] [PMID: 2479133]
Mink, J.W. The basal ganglia: focused selection and inhibition of competing motor programs. Prog. Neurobiol., 1996, 50(4), 381-425.
[] [PMID: 9004351]
Redgrave, P.; Prescott, T.J.; Gurney, K. The basal ganglia: a vertebrate solution to the selection problem? Neuroscience, 1999, 89(4), 1009-1023.
[] [PMID: 10362291]
Graybiel, A.M.; Aosaki, T.; Flaherty, A.W.; Kimura, M. The basal ganglia and adaptive motor control. Science, 1994, 265(5180), 1826-1831.
[] [PMID: 8091209]
Marsden, C.D.; Obeso, J.A. The functions of the basal ganglia and the paradox of stereotaxic surgery in Parkinson’s disease. Brain, 1994, 117(Pt 4), 877-897.
[] [PMID: 7922472]
Brooks, D.J. The role of the basal ganglia in motor control: contributions from PET. J. Neurol. Sci., 1995, 128(1), 1-13.
[] [PMID: 7722526]
Wichmann, T.; DeLong, M.R. Functional neuroanatomy of the basal ganglia in Parkinson’s disease. Adv. Neurol., 2003, 91, 9-18.
[PMID: 12442660]
Wickens, J.R.; Horvitz, J.C.; Costa, R.M.; Killcross, S.; Killcross, S. Dopaminergic mechanisms in actions and habits. J. Neurosci., 2007, 27(31), 8181-8183.
[] [PMID: 17670964]
DeLong, M.R.; Wichmann, T.; Wichmann, T. Circuits and circuit disorders of the basal ganglia. Arch. Neurol., 2007, 64(1), 20-24.
[] [PMID: 17210805]
Jankovic, J. Parkinson’s disease: clinical features and diagnosis. J. Neurol. Neurosurg. Psychiatry, 2008, 79(4), 368-376.
[] [PMID: 18344392]
Packard, M.G.; Knowlton, B.J. Learning and memory functions of the Basal Ganglia. Annu. Rev. Neurosci., 2002, 25, 563-593.
[] [PMID: 12052921]
Goodman, J.; Packard, M.G. The role of the dorsal striatum in extinction: A memory systems perspective. Neurobiol. Learn. Mem., 2018, 150, 48-55.
[] [PMID: 29501803]
Yager, L.M.; Garcia, A.F.; Wunsch, A.M.; Ferguson, S.M. The ins and outs of the striatum: role in drug addiction. Neuroscience, 2015, 301, 529-541.
[] [PMID: 26116518]
Balleine, B.W.; Delgado, M.R.; Hikosaka, O. The role of the dorsal striatum in reward and decision-making. J. Neurosci., 2007, 27(31), 8161-8165.
[] [PMID: 17670959]
Schneider, J.S.; Lidsky, T.I. Processing of somatosensory information in striatum of behaving cats. J. Neurophysiol., 1981, 45(5), 841-851.
[] [PMID: 7241172]
Chudler, E.H. Response properties of neurons in the caudate-putamen and globus pallidus to noxious and non-noxious thermal stimulation in anesthetized rats. Brain Res., 1998, 812(1-2), 283-288.
[] [PMID: 9813370]
Richards, C.D.; Taylor, D.C. Electrophysiological evidence for a somatotopic sensory projection to the striatum of the rat. Neurosci. Lett., 1982, 30(3), 235-240.
[] [PMID: 7050770]
Chudler, E.H.; Sugiyama, K.; Dong, W.K. Nociceptive responses in the neostriatum and globus pallidus of the anesthetized rat. J. Neurophysiol., 1993, 69(6), 1890-1903.
[] [PMID: 8350129]
Casey, K.L.; Minoshima, S.; Morrow, T.J.; Koeppe, R.A. Comparison of human cerebral activation pattern during cutaneous warmth, heat pain, and deep cold pain. J. Neurophysiol., 1996, 76(1), 571-581.
[] [PMID: 8836245]
Svensson, P.; Minoshima, S.; Beydoun, A.; Morrow, T.J.; Casey, K.L. Cerebral processing of acute skin and muscle pain in humans. J. Neurophysiol., 1997, 78(1), 450-460.
[] [PMID: 9242293]
Coghill, R.C.; McHaffie, J.G.; Yen, Y.F. Neural correlates of interindividual differences in the subjective experience of pain. Proc. Natl. Acad. Sci. USA, 2003, 100(14), 8538-8542.
[] [PMID: 12824463]
Magnusson, J.E.; Fisher, K. The involvement of dopamine in nociception: the role of D(1) and D(2) receptors in the dorsolateral striatum. Brain Res., 2000, 855(2), 260-266.
[] [PMID: 10677598]
Gear, R.W.; Levine, J.D. Rostral ventral medulla cholinergic mechanism in pain-induced analgesia. Neurosci. Lett., 2009, 464(3), 170-172.
[] [PMID: 19699268]
Barceló, A.C.; Filippini, B.; Pazo, J.H. The striatum and pain modulation. Cell. Mol. Neurobiol., 2012, 32(1), 1-12.
[] [PMID: 21789630]
Nakamura, Y.; Izumi, H.; Shimizu, T.; Hisaoka-Nakashima, K.; Morioka, N.; Nakata, Y. Volume transmission of substance P in striatum induced by intraplantar formalin injection attenuates nociceptive responses via activation of the neurokinin 1 receptor. J. Pharmacol. Sci., 2013, 121(4), 257-271.
[] [PMID: 23514787]
Gerdelat-Mas, A.; Simonetta-Moreau, M.; Thalamas, C.; Ory-Magne, F.; Slaoui, T.; Rascol, O.; Brefel-Courbon, C. Levodopa raises objective pain threshold in Parkinson’s disease: a RIII reflex study. J. Neurol. Neurosurg. Psychiatry, 2007, 78(10), 1140-1142.
[] [PMID: 17504881]
Nolano, M.; Provitera, V.; Estraneo, A.; Selim, M.M.; Caporaso, G.; Stancanelli, A.; Saltalamacchia, A.M.; Lanzillo, B.; Santoro, L. Sensory deficit in Parkinson’s disease: evidence of a cutaneous denervation. Brain, 2008, 131(Pt 7), 1903-1911.
[] [PMID: 18515869]
Perrotta, A.; Serpino, C.; Cormio, C.; Serrao, M.; Sandrini, G.; Pierelli, F.; de Tommaso, M. Abnormal spinal cord pain processing in Huntington’s disease. The role of the diffuse noxious inhibitory control. Clin. Neurophysiol., 2012, 123(8), 1624-1630.
[] [PMID: 22341978]
Hebert, G.W.; Baumeister, A.A.; Nagy, M. The antinociceptive effect of intranigral injection of morphine in ketamine- and halothane-anesthetized rats. Neuropharmacology, 1990, 29(8), 771-777.
[] [PMID: 2274112]
Parent, A.; Côté, P.Y.; Lavoie, B. Chemical anatomy of primate basal ganglia. Prog. Neurobiol., 1995, 46(2-3), 131-197.
[] [PMID: 7568912]
Van Waes, V.; Beverley, J.A.; Siman, H.; Tseng, K.Y.; Steiner, H. CB1 cannabinoid receptor expression in the striatum: Association with corticostriatal circuits and developmental regulation. Front. Pharmacol., 2012, 3, 21.
[] [PMID: 22416230]
Rossi, F.; Marabese, I.; De Chiaro, M.; Boccella, S.; Luongo, L.; Guida, F.; De Gregorio, D.; Giordano, C.; de Novellis, V.; Palazzo, E.; Maione, S. Dorsal striatum metabotropic glutamate receptor 8 affects nocifensive responses and rostral ventromedial medulla cell activity in neuropathic pain conditions. J. Neurophysiol., 2014, 111(11), 2196-2209.
[] [PMID: 24304862]
Marabese, I.; Boccella, S.; Iannotta, M.; Luongo, L.; de Novellis, V.; Guida, F.; Serra, N.; Farina, A.; Maione, S.; Palazzo, E. Metabotropic glutamate receptor subtype 7 in the dorsal striatum oppositely modulates pain in sham and neuropathic rats. Neuropharmacology, 2018, 135, 86-99.
[] [PMID: 29505788]
Leite-Almeida, H.; Valle-Fernandes, A.; Almeida, A. Brain projections from the medullary dorsal reticular nucleus: an anterograde and retrograde tracing study in the rat. Neuroscience, 2006, 140(2), 577-595.
[] [PMID: 16563637]
Blandini, F.; Garcia-Osuna, M.; Greenamyre, J.T. Subthalamic ablation reverses changes in basal ganglia oxidative metabolism and motor response to apomorphine induced by nigrostriatal lesion in rats. Eur. J. Neurosci., 1997, 9(7), 1407-1413.
[] [PMID: 9240398]
Osikowicz, M.; Mika, J.; Przewlocka, B. The glutamatergic system as a target for neuropathic pain relief. Exp. Physiol., 2013, 98(2), 372-384.
[] [PMID: 23002244]
Vardi, N.; Duvoisin, R.; Wu, G.; Sterling, P. Localization of mGluR6 to dendrites of ON bipolar cells in primate retina. J. Comp. Neurol., 2000, 423(3), 402-412.
[<402:AID-CNE4>3.0.CO;2-E] [PMID: 10870081]
Kosinski, C.M.; Risso Bradley, S.; Conn, P.J.; Levey, A.I.; Landwehrmeyer, G.B.; Penney, J.B., Jr; Young, A.B.; Standaert, D.G. Localization of metabotropic glutamate receptor 7 mRNA and mGluR7a protein in the rat basal ganglia. J. Comp. Neurol., 1999, 415(2), 266-284.
[ 415:2<266:AID-CNE9>3.0.CO;2-7] [PMID: 10545164]
Cartmell, J.; Schoepp, D.D. Regulation of neurotransmitter release by metabotropic glutamate receptors. J. Neurochem., 2000, 75(3), 889-907.
[] [PMID: 10936169]
Niswender, C.M.; Johnson, K.A.; Luo, Q.; Ayala, J.E.; Kim, C.; Conn, P.J.; Weaver, C.D. A novel assay of Gi/o-linked G protein-coupled receptor coupling to potassium channels provides new insights into the pharmacology of the group III metabotropic glutamate receptors. Mol. Pharmacol., 2008, 73(4), 1213-1224.
[] [PMID: 18171729]
Engers, D.W.; Niswender, C.M.; Weaver, C.D.; Jadhav, S.; Menon, U.N.; Zamorano, R.; Conn, P.J.; Lindsley, C.W.; Hopkins, C.R. Synthesis and evaluation of a series of heterobiarylamides that are centrally penetrant metabotropic glutamate receptor 4 (mGluR4) positive allosteric modulators (PAMs). J. Med. Chem., 2009, 52(14), 4115-4118.
[] [PMID: 19469556]
Bradley, S.R.; Standaert, D.G.; Levey, A.I.; Conn, P.J. Distribution of group III mGluRs in rat basal ganglia with subtype-specific antibodies. Ann. N. Y. Acad. Sci., 1999, 868, 531-534.
[] [PMID: 10414330]
Corti, C.; Aldegheri, L.; Somogyi, P.; Ferraguti, F. Distribution and synaptic localisation of the metabotropic glutamate receptor 4 (mGluR4) in the rodent CNS. Neuroscience, 2002, 110(3), 403-420.
[] [PMID: 11906782]
Akira, S.; Takeda, K.; Kaisho, T. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat. Immunol., 2001, 2(8), 675-680.
[] [PMID: 11477402]
Nicoletti, F.; Bockaert, J.; Collingridge, G.L.; Conn, P.J.; Ferraguti, F.; Schoepp, D.D.; Wroblewski, J.T.; Pin, J.P. Metabotropic glutamate receptors: from the workbench to the bedside. Neuropharmacology, 2011, 60(7-8), 1017-1041.
[] [PMID: 21036182]
Akiba, Y.; Watanabe, C.; Mizumori, M.; Kaunitz, J.D. Luminal L-glutamate enhances duodenal mucosal defense mechanisms via multiple glutamate receptors in rats. Am. J. Physiol. Gastrointest. Liver Physiol., 2009, 297(4), G781-G791.
[] [PMID: 19643955]
Nakamura, E.; Hasumura, M.; San, G.A.; Uneyama, H.; Torii, K. New frontiers in gut nutrient sensor research: luminal glutamate-sensing cells in rat gastric mucosa. J. Pharmacol. Sci., 2010, 112(1), 13-18.
[] [PMID: 20093783]
Chang, H.J.; Yoo, B.C.; Lim, S.B.; Jeong, S.Y.; Kim, W.H.; Park, J.G. Metabotropic glutamate receptor 4 expression in colorectal carcinoma and its prognostic significance. Clin. Cancer Res., 2005, 11(9), 3288-3295.
[] [PMID: 15867225]
Zhang, Z.; Liu, Y.; Wang, K.; Zhu, K.; Zheng, X.; Wang, L.; Luan, Y.; Wang, X.; Lu, H.; Wu, K.; Chen, X.; He, D.; Liu, Y. Activation of type 4 metabotropic glutamate receptor promotes cell apoptosis and inhibits proliferation in bladder cancer. J. Cell. Physiol., 2019, 234(3), 2741-2755.
[] [PMID: 30145816]
Uehara, S.; Muroyama, A.; Echigo, N.; Morimoto, R.; Otsuka, M.; Yatsushiro, S.; Moriyama, Y. Metabotropic glutamate receptor type 4 is involved in autoinhibitory cascade for glucagon secretion by alpha-cells of islet of Langerhans. Diabetes, 2004, 53(4), 998-1006.
[] [PMID: 15047615]
Sarría, R.; Díez, J.; Losada, J.; Doñate-Oliver, F.; Kuhn, R.; Grandes, P. Immunocytochemical localization of metabotropic (mGluR2/3 and mGluR4a) and ionotropic (GluR2/3) glutamate receptors in adrenal medullary ganglion cells. Histol. Histopathol., 2006, 21(2), 141-147.
[PMID: 16329038]
Fallarino, F.; Volpi, C.; Fazio, F.; Notartomaso, S.; Vacca, C.; Busceti, C.; Bicciato, S.; Battaglia, G.; Bruno, V.; Puccetti, P.; Fioretti, M.C.; Nicoletti, F.; Grohmann, U.; Di Marco, R. Metabotropic glutamate receptor-4 modulates adaptive immunity and restrains neuroinflammation. Nat. Med., 2010, 16(8), 897-902.
[] [PMID: 20657581]
Volpi, C.; Fallarino, F.; Mondanelli, G.; Macchiarulo, A.; Grohmann, U. Opportunities and challenges in drug discovery targeting metabotropic glutamate receptor 4. Expert Opin. Drug Discov., 2018, 13(5), 411-423.
[] [PMID: 29486616]
Thomsen, C. The L-AP4 receptor. Gen. Pharmacol., 1997, 29(2), 151-158.
[] [PMID: 9251893]
Pekhletski, R.; Gerlai, R.; Overstreet, L.S.; Huang, X.P.; Agopyan, N.; Slater, N.T.; Abramow-Newerly, W.; Roder, J.C.; Hampson, D.R. Impaired cerebellar synaptic plasticity and motor performance in mice lacking the mGluR4 subtype of metabotropic glutamate receptor. J. Neurosci., 1996, 16(20), 6364-6373.
[] [PMID: 8815915]
Davis, M.J.; Haley, T.; Duvoisin, R.M.; Raber, J. Measures of anxiety, sensorimotor function, and memory in male and female mGluR4/ mice. Behav. Brain Res., 2012, 229(1), 21-28.
[] [PMID: 22227508]
Gerlai, R.; Roder, J.C.; Hampson, D.R. Altered spatial learning and memory in mice lacking the mGluR4 subtype of metabotropic glutamate receptor. Behav. Neurosci., 1998, 112(3), 525-532.
[] [PMID: 9676970]
Blednov, Y.A.; Walker, D.; Osterndorf-Kahanek, E.; Harris, R.A. Mice lacking metabotropic glutamate receptor 4 do not show the motor stimulatory effect of ethanol. Alcohol, 2004, 34(2-3), 251-259.
[] [PMID: 15902920]
Flor, P.J.; Acher, F.C. Orthosteric versus allosteric GPCR activation: the great challenge of group-III mGluRs. Biochem. Pharmacol., 2012, 84(4), 414-424.
[] [PMID: 22554564]
Wierońska, J.M.; Stachowicz, K.; Acher, F.; Lech, T.; Pilc, A. Opposing efficacy of group III mGlu receptor activators, LSP1-2111 and AMN082, in animal models of positive symptoms of schizophrenia. Psychopharmacology (Berl.), 2012, 220(3), 481-494.
[] [PMID: 21952670]
Wierońska, J.M.; Stachowicz, K.; Pałucha-Poniewiera, A.; Acher, F.; Brański, P.; Pilc, A. Metabotropic glutamate receptor 4 novel agonist LSP1-2111 with anxiolytic, but not antidepressant-like activity, mediated by serotonergic and GABAergic systems. Neuropharmacology, 2010, 59(7-8), 627-634.
[] [PMID: 20713068]
Goudet, C.; Vilar, B.; Courtiol, T.; Deltheil, T.; Bessiron, T.; Brabet, I.; Oueslati, N.; Rigault, D.; Bertrand, H.O.; McLean, H.; Daniel, H.; Amalric, M.; Acher, F.; Pin, J.P. A novel selective metabotropic glutamate receptor 4 agonist reveals new possibilities for developing subtype selective ligands with therapeutic potential. FASEB J., 2012, 26(4), 1682-1693.
[] [PMID: 22223752]
Vilar, B.; Busserolles, J.; Ling, B.; Laffray, S.; Ulmann, L.; Malhaire, F.; Chapuy, E.; Aissouni, Y.; Etienne, M.; Bourinet, E.; Acher, F.; Pin, J.P.; Eschalier, A.; Goudet, C. Alleviating pain hypersensitivity through activation of type 4 metabotropic glutamate receptor. J. Neurosci., 2013, 33(48), 18951-18965.
[] [PMID: 24285900]
Podkowa, K.; Rzeźniczek, S.; Marciniak, M.; Acher, F.; Pilc, A.; Pałucha-Poniewiera, A. A novel mGlu4 selective agonist LSP4-2022 increases behavioral despair in mouse models of antidepressant action. Neuropharmacology, 2015, 97, 338-345.
[] [PMID: 26074092]
Woźniak, M.; Gołembiowska, K.; Noworyta-Sokołowska, K.; Acher, F.; Cieślik, P.; Kusek, M.; Tokarski, K.; Pilc, A.; Wierońska, J.M. Neurochemical and behavioral studies on the 5-HT1A-dependent antipsychotic action of the mGlu4 receptor agonist LSP4-2022. Neuropharmacology, 2017, 115, 149-165.
[] [PMID: 27465045]
Maj, M.; Bruno, V.; Dragic, Z.; Yamamoto, R.; Battaglia, G.; Inderbitzin, W.; Stoehr, N.; Stein, T.; Gasparini, F.; Vranesic, I.; Kuhn, R.; Nicoletti, F.; Flor, P.J. (-)-PHCCC, a positive allosteric modulator of mGluR4: characterization, mechanism of action, and neuroprotection. Neuropharmacology, 2003, 45(7), 895-906.
[] [PMID: 14573382]
Marino, M.J.; Williams, D.L., Jr; O’Brien, J.A.; Valenti, O.; McDonald, T.P.; Clements, M.K.; Wang, R.; DiLella, A.G.; Hess, J.F.; Kinney, G.G.; Conn, P.J. Allosteric modulation of group III metabotropic glutamate receptor 4: a potential approach to Parkinson’s disease treatment. Proc. Natl. Acad. Sci. USA, 2003, 100(23), 13668-13673.
[] [PMID: 14593202]
Le Poul, E.; Boléa, C.; Girard, F.; Poli, S.; Charvin, D.; Campo, B.; Bortoli, J.; Bessif, A.; Luo, B.; Koser, A.J.; Hodge, L.M.; Smith, K.M.; DiLella, A.G.; Liverton, N.; Hess, F.; Browne, S.E.; Reynolds, I.J. A potent and selective metabotropic glutamate receptor 4 positive allosteric modulator improves movement in rodent models of Parkinson’s disease. J. Pharmacol. Exp. Ther., 2012, 343(1), 167-177.
[] [PMID: 22787118]
Charvin, D.; Pomel, V.; Ortiz, M.; Frauli, M.; Scheffler, S.; Steinberg, E.; Baron, L.; Deshons, L.; Rudigier, R.; Thiarc, D.; Morice, C.; Manteau, B.; Mayer, S.; Graham, D.; Giethlen, B.; Brugger, N.; Hédou, G.; Conquet, F.; Schann, S. Discovery, structure-activity relationship, and antiparkinsonian effect of a potent and brain-penetrant chemical series of positive allosteric modulators of metabotropic glutamate receptor 4. J. Med. Chem., 2017, 60(20), 8515-8537.
[] [PMID: 28902994]
Smith, Y.; Wichmann, T.; Factor, S.A.; DeLong, M.R. Parkinson’s disease therapeutics: new developments and challenges since the introduction of levodopa. Neuropsychopharmacology, 2012, 37(1), 213-246.
[] [PMID: 21956442]
Conn, P.J.; Lindsley, C.W.; Meiler, J.; Niswender, C.M. Opportunities and challenges in the discovery of allosteric modulators of GPCRs for treating CNS disorders. Nat. Rev. Drug Discov., 2014, 13(9), 692-708.
[] [PMID: 25176435]
Amalric, M. Targeting metabotropic glutamate receptors (mGluRs) in Parkinson’s disease. Curr. Opin. Pharmacol., 2015, 20, 29-34.
[] [PMID: 25462289]
Litim, N.; Morissette, M.; Di Paolo, T. Metabotropic glutamate receptors as therapeutic targets in Parkinson’s disease: An update from the last 5 years of research. Neuropharmacology, 2017, 115, 166-179.
[] [PMID: 27055772]
Maksymetz, J.; Moran, S.P.; Conn, P.J. Targeting metabotropic glutamate receptors for novel treatments of schizophrenia. Mol. Brain, 2017, 10(1), 15.
[] [PMID: 28446243]
Davis, M.J.; Duvoisin, R.M.; Raber, J. Related functions of mGlu4 and mGlu8. Pharmacol. Biochem. Behav., 2013, 111, 11-16.
[] [PMID: 23948069]
Célanire, S.; Campo, B. Recent advances in the drug discovery of metabotropic glutamate receptor 4 (mGluR4) activators for the treatment of CNS and non-CNS disorders. Expert Opin. Drug Discov., 2012, 7(3), 261-280.
[] [PMID: 22468956]
Pałucha-Poniewiera, A.; Novák, K.; Pilc, A. Group III mGlu receptor agonist, ACPT-I, attenuates morphine-withdrawal symptoms after peripheral administration in mice. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2009, 33(8), 1454-1457.
[] [PMID: 19660510]
Zaniewska, M.; Przegaliński, E.; Filip, M.; Pilc, A.; Doller, D. Inhibitory actions of mGlu4 receptor ligands on cocaine-, but not nicotine-, induced sensitizing and conditioning locomotor responses in rats. Pharmacol. Rep., 2014, 66(2), 205-211.
[] [PMID: 24911071]
Fendt, M.; Schmid, S.; Thakker, D.R.; Jacobson, L.H.; Yamamoto, R.; Mitsukawa, K.; Maier, R.; Natt, F.; Hüsken, D.; Kelly, P.H.; McAllister, K.H.; Hoyer, D.; van der Putten, H.; Cryan, J.F.; Flor, P.J. mGluR7 facilitates extinction of aversive memories and controls amygdala plasticity. Mol. Psychiatry, 2008, 13(10), 970-979.
[] [PMID: 17712315]
Rovira, X.; Trapero, A.; Pittolo, S.; Zussy, C.; Faucherre, A.; Jopling, C.; Giraldo, J.; Pin, J.P.; Gorostiza, P.; Goudet, C.; Llebaria, A. OptoGluNAM4.1, a photoswitchable allosteric antagonist for real-time control of mGlu4 receptor activity. Cell Chem. Biol., 2016, 23(8), 929-934.
[] [PMID: 27478159]
Fallarino, F.; Bianchi, R.; Orabona, C.; Vacca, C.; Belladonna, M.L.; Fioretti, M.C.; Serreze, D.V.; Grohmann, U.; Puccetti, P. CTLA-4-Ig activates forkhead transcription factors and protects dendritic cells from oxidative stress in nonobese diabetic mice. J. Exp. Med., 2004, 200(8), 1051-1062.
[] [PMID: 15492127]
Besong, G.; Battaglia, G.; D’Onofrio, M.; Di Marco, R.; Ngomba, R.T.; Storto, M.; Castiglione, M.; Mangano, K.; Busceti, C.L.; Nicoletti, F.R.; Bacon, K.; Tusche, M.; Valenti, O.; Conn, P.J.; Bruno, V.; Nicoletti, F. Activation of Group III Metabotropic Glutamate Receptors Inhibits the Production of RANTES in Glial Cell Cultures. J. Neurosci., 2002, 22, 5403-5411.
Young, R.L.; Cooper, N.J.; Blackshaw, L.A. Anatomy and function of group III metabotropic glutamate receptors in gastric vagal pathways. Neuropharmacology, 2008, 54(6), 965-975.
[] [PMID: 18371991]
Filpa, V.; Moro, E.; Protasoni, M.; Crema, F.; Frigo, G.; Giaroni, C. Role of glutamatergic neurotransmission in the enteric nervous system and brain-gut axis in health and disease. Neuropharmacology, 2016, 111, 14-33.
[] [PMID: 27561972]
Ngomba, R.T.; Ferraguti, F.; Badura, A.; Citraro, R.; Santolini, I.; Battaglia, G.; Bruno, V.; De Sarro, G.; Simonyi, A.; van Luijtelaar, G.; Nicoletti, F. Positive allosteric modulation of metabotropic glutamate 4 (mGlu4) receptors enhances spontaneous and evoked absence seizures. Neuropharmacology, 2008, 54(2), 344-354.
[] [PMID: 18022649]
Cuomo, D.; Martella, G.; Barabino, E.; Platania, P.; Vita, D.; Madeo, G.; Selvam, C.; Goudet, C.; Oueslati, N.; Pin, J.P.; Acher, F.; Pisani, A.; Beurrier, C.; Melon, C.; Kerkerian-Le Goff, L.; Gubellini, P. Metabotropic glutamate receptor subtype 4 selectively modulates both glutamate and GABA transmission in the striatum: implications for Parkinson’s disease treatment. J. Neurochem., 2009, 109(4), 1096-1105.
[] [PMID: 19519781]
Bennouar, K.E.; Uberti, M.A.; Melon, C.; Bacolod, M.D.; Jimenez, H.N.; Cajina, M.; Kerkerian-Le Goff, L.; Doller, D.; Gubellini, P. Synergy between L-DOPA and a novel positive allosteric modulator of metabotropic glutamate receptor 4: implications for Parkinson’s disease treatment and dyskinesia. Neuropharmacology, 2013, 66, 158-169.
[] [PMID: 22491024]
Gubellini, P.; Melon, C.; Dale, E.; Doller, D.; Kerkerian-Le Goff, L. Distinct effects of mGlu4 receptor positive allosteric modulators at corticostriatal vs. striatopallidal synapses may differentially contribute to their antiparkinsonian action. Neuropharmacology, 2014, 85, 166-177.
[] [PMID: 24866785]
Iskhakova, L.; Smith, Y. mGluR4-containing corticostriatal terminals: synaptic interactions with direct and indirect pathway neurons in mice. Brain Struct. Funct., 2016, 221(9), 4589-4599.
[] [PMID: 26832920]
Yin, S.; Noetzel, M.J.; Johnson, K.A.; Zamorano, R.; Jalan-Sakrikar, N.; Gregory, K.J.; Conn, P.J.; Niswender, C.M. Selective actions of novel allosteric modulators reveal functional heteromers of metabotropic glutamate receptors in the CNS. J. Neurosci., 2014, 34(1), 79-94.
[] [PMID: 24381270]
Durieux, P.F.; Bearzatto, B.; Guiducci, S.; Buch, T.; Waisman, A.; Zoli, M.; Schiffmann, S.N.; de Kerchove d’Exaerde, A. D2R striatopallidal neurons inhibit both locomotor and drug reward processes. Nat. Neurosci., 2009, 12(4), 393-395.
[] [PMID: 19270687]
Bateup, H.S.; Santini, E.; Shen, W.; Birnbaum, S.; Valjent, E.; Surmeier, D.J.; Fisone, G.; Nestler, E.J.; Greengard, P. Distinct subclasses of medium spiny neurons differentially regulate striatal motor behaviors. Proc. Natl. Acad. Sci. USA, 2010, 107(33), 14845-14850.
[] [PMID: 20682746]
Kravitz, A.V.; Freeze, B.S.; Parker, P.R.; Kay, K.; Thwin, M.T.; Deisseroth, K.; Kreitzer, A.C. Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature, 2010, 466(7306), 622-626.
[] [PMID: 20613723]
Cui, G.; Jun, S.B.; Jin, X.; Pham, M.D.; Vogel, S.S.; Lovinger, D.M.; Costa, R.M. Concurrent activation of striatal direct and indirect pathways during action initiation. Nature, 2013, 494(7436), 238-242.
[] [PMID: 23354054]
Bradley, S.R.; Levey, A.I.; Hersch, S.M.; Conn, P.J. Immunocytochemical localization of group III metabotropic glutamate receptors in the hippocampus with subtype-specific antibodies. J. Neurosci., 1996, 16(6), 2044-2056.
[] [PMID: 8604049]
Duty, S. Therapeutic potential of targeting group III metabotropic glutamate receptors in the treatment of Parkinson’s disease. Br. J. Pharmacol., 2010, 161(2), 271-287.
[] [PMID: 20735415]
Bogenpohl, J.; Galvan, A.; Hu, X.; Wichmann, T.; Smith, Y. Metabotropic glutamate receptor 4 in the basal ganglia of parkinsonian monkeys: ultrastructural localization and electrophysiological effects of activation in the striatopallidal complex. Neuropharmacology, 2013, 66, 242-252.
[] [PMID: 22634360]
Beurrier, C.; Lopez, S.; Révy, D.; Selvam, C.; Goudet, C.; Lhérondel, M.; Gubellini, P.; Kerkerian-LeGoff, L.; Acher, F.; Pin, J.P.; Amalric, M. Electrophysiological and behavioral evidence that modulation of metabotropic glutamate receptor 4 with a new agonist reverses experimental parkinsonism. FASEB J., 2009, 23(10), 3619-3628.
[] [PMID: 19525404]
Battaglia, G.; Busceti, C.L.; Molinaro, G.; Biagioni, F.; Traficante, A.; Nicoletti, F.; Bruno, V. Pharmacological activation of mGlu4 metabotropic glutamate receptors reduces nigrostriatal degeneration in mice treated with 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. J. Neurosci., 2006, 26(27), 7222-7229.
[] [PMID: 16822979]
Broadstock, M.; Austin, P.J.; Betts, M.J.; Duty, S. Antiparkinsonian potential of targeting group III metabotropic glutamate receptor subtypes in the rodent substantia nigra pars reticulata. Br. J. Pharmacol., 2012, 165(4b), 1034-1045.
[] [PMID: 21627638]
Betts, M.J.; O’Neill, M.J.; Duty, S. Allosteric modulation of the group III mGlu4 receptor provides functional neuroprotection in the 6-hydroxydopamine rat model of Parkinson’s disease. Br. J. Pharmacol., 2012, 166(8), 2317-2330.
[] [PMID: 22404342]
Bruno, V.; Battaglia, G.; Ksiazek, I.; van der Putten, H.; Catania, M.V.; Giuffrida, R.; Lukic, S.; Leonhardt, T.; Inderbitzin, W.; Gasparini, F.; Kuhn, R.; Hampson, D.R.; Nicoletti, F.; Flor, P.J. Selective activation of mGlu4 metabotropic glutamate receptors is protective against excitotoxic neuronal death. J. Neurosci., 2000, 20(17), 6413-6420.
[] [PMID: 10964947]
Usoskin, D.; Furlan, A.; Islam, S.; Abdo, H.; Lönnerberg, P.; Lou, D.; Hjerling-Leffler, J.; Haeggström, J.; Kharchenko, O.; Kharchenko, P.V.; Linnarsson, S.; Ernfors, P. Unbiased classification of sensory neuron types by large-scale single-cell RNA sequencing. Nat. Neurosci., 2015, 18(1), 145-153.
[] [PMID: 25420068]
Valerio, A.; Paterlini, M.; Boifava, M.; Memo, M.; Spano, P. Metabotropic glutamate receptor mRNA expression in rat spinal cord. Neuroreport, 1997, 8(12), 2695-2699.
[] [PMID: 9295103]
Azkue, J.J.; Murga, M.; Fernández-Capetillo, O.; Mateos, J.M.; Elezgarai, I.; Benítez, R.; Osorio, A.; Díez, J.; Puente, N.; Bilbao, A.; Bidaurrazaga, A.; Kuhn, R.; Grandes, P. Immunoreactivity for the group III metabotropic glutamate receptor subtype mGluR4a in the superficial laminae of the rat spinal dorsal horn. J. Comp. Neurol., 2001, 430(4), 448-457.
[<448:AID-CNE1042>3.0.CO;2-O] [PMID: 11169479]
Goudet, C.; Chapuy, E.; Alloui, A.; Acher, F.; Pin, J.P.; Eschalier, A. Group III metabotropic glutamate receptors inhibit hyperalgesia in animal models of inflammation and neuropathic pain. Pain, 2008, 137(1), 112-124.
[] [PMID: 17900808]
Wang, H.; Jiang, W.; Yang, R.; Li, Y. Spinal metabotropic glutamate receptor 4 is involved in neuropathic pain. Neuroreport, 2011, 22(5), 244-248.
[] [PMID: 21358553]
Corti, C.; Restituito, S.; Rimland, J.M.; Brabet, I.; Corsi, M.; Pin, J.P.; Ferraguti, F. Cloning and characterization of alternative mRNA forms for the rat metabotropic glutamate receptors mGluR7 and mGluR8. Eur. J. Neurosci., 1998, 10(12), 3629-3641.
[] [PMID: 9875342]
Kinoshita, A.; Shigemoto, R.; Ohishi, H.; van der Putten, H.; Mizuno, N. 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., 1998, 393(3), 332-352.
[<332: AID-CNE6>3.0.CO;2-2] [PMID: 9548554]
Messenger, M.J.; Dawson, L.G.; Duty, S. Changes in metabotropic glutamate receptor 1-8 gene expression in the rodent basal ganglia motor loop following lesion of the nigrostriatal tract. Neuropharmacology, 2002, 43(2), 261-271.
[] [PMID: 12213280]
Dev, K.K.; Nakanishi, S.; Henley, J.M. Regulation of mglu(7) receptors by proteins that interact with the intracellular C-terminus. Trends Pharmacol. Sci., 2001, 22(7), 355-361.
[] [PMID: 11431030]
Schulz, H.L.; Stohr, H.; Weber, B.H. Characterization of three novel isoforms of the metabotrobic glutamate receptor 7 (GRM7). Neurosci. Lett., 2002, 326(1), 37-40.
[] [PMID: 12052533]
Ohishi, H.; Nomura, S.; Ding, Y.Q.; Shigemoto, R.; Wada, E.; Kinoshita, A.; Li, J.L.; Neki, A.; Nakanishi, S.; Mizuno, N. Presynaptic localization of a metabotropic glutamate receptor, mGluR7, in the primary afferent neurons: an immunohistochemical study in the rat. Neurosci. Lett., 1995, 202(1-2), 85-88.
[] [PMID: 8787837]
Shigemoto, R.; Kulik, A.; Roberts, J.D.; Ohishi, H.; Nusser, Z.; Kaneko, T.; Somogyi, P. Target-cell-specific concentration of a metabotropic glutamate receptor in the presynaptic active zone. Nature, 1996, 381(6582), 523-525.
[] [PMID: 8632825]
Dalezios, Y.; Luján, R.; Shigemoto, R.; Roberts, J.D.; Somogyi, P. Enrichment of mGluR7a in the presynaptic active zones of GABAergic and non-GABAergic terminals on interneurons in the rat somatosensory cortex. Cereb. Cortex, 2002, 12(9), 961-974.
[] [PMID: 12183395]
Somogyi, P.; Dalezios, Y.; Luján, R.; Roberts, J.D.; Watanabe, M.; Shigemoto, R. High level of mGluR7 in the presynaptic active zones of select populations of GABAergic terminals innervating interneurons in the rat hippocampus. Eur. J. Neurosci., 2003, 17(12), 2503-2520.
[] [PMID: 12823458]
Niswender, C.M.; Conn, P.J. Metabotropic glutamate receptors: physiology, pharmacology, and disease. Annu. Rev. Pharmacol. Toxicol., 2010, 50, 295-322.
[] [PMID: 20055706]
Cryan, J.F.; Kelly, P.H.; Neijt, H.C.; Sansig, G.; Flor, P.J.; van Der Putten, H. Antidepressant and anxiolytic-like effects in mice lacking the group III metabotropic glutamate receptor mGluR7. Eur. J. Neurosci., 2003, 17(11), 2409-2417.
[] [PMID: 12814372]
Callaerts-Vegh, Z.; Beckers, T.; Ball, S.M.; Baeyens, F.; Callaerts, P.F.; Cryan, J.F.; Molnar, E.; D’Hooge, R. Concomitant deficits in working memory and fear extinction are functionally dissociated from reduced anxiety in metabotropic glutamate receptor 7-deficient mice. J. Neurosci., 2006, 26(24), 6573-6582.
[] [PMID: 16775145]
Masugi, M.; Yokoi, M.; Shigemoto, R.; Muguruma, K.; Watanabe, Y.; Sansig, G.; van der Putten, H.; Nakanishi, S. Metabotropic glutamate receptor subtype 7 ablation causes deficit in fear response and conditioned taste aversion. J. Neurosci., 1999, 19(3), 955-963.
[] [PMID: 9920659]
Goddyn, H.; Callaerts-Vegh, Z.; Stroobants, S.; Dirikx, T.; Vansteenwegen, D.; Hermans, D.; van der Putten, H.; D’Hooge, R. Deficits in acquisition and extinction of conditioned responses in mGluR7 knockout mice. Neurobiol. Learn. Mem., 2008, 90(1), 103-111.
[] [PMID: 18289889]
Goddyn, H.; Callaerts-Vegh, Z.; D’Hooge, R. Functional dissociation of group III metabotropic glutamate receptors revealed by direct comparison between the behavioral profiles of knockout mouse lines. Int. J. Neuropsychopharmacol., 2015, 18(11)pyv053
[] [PMID: 25999589]
Mitsukawa, K.; Yamamoto, R.; Ofner, S.; Nozulak, J.; Pescott, O.; Lukic, S.; Stoehr, N.; Mombereau, C.; Kuhn, R.; McAllister, K.H.; van der Putten, H.; Cryan, J.F.; Flor, P.J. A selective metabotropic glutamate receptor 7 agonist: activation of receptor signaling via an allosteric site modulates stress parameters in vivo. Proc. Natl. Acad. Sci. USA, 2005, 102(51), 18712-18717.
[] [PMID: 16339898]
Stachowicz, K.; Brañski, P.; Kłak, K.; van der Putten, H.; Cryan, J.F.; Flor, P.J.; Andrzej, P. Selective activation of metabotropic G-protein-coupled glutamate 7 receptor elicits anxiolytic-like effects in mice by modulating GABAergic neurotransmission. Behav. Pharmacol., 2008, 19(5-6), 597-603.
[] [PMID: 18690114]
Bradley, S.R.; Uslaner, J.M.; Flick, R.B.; Lee, A.; Groover, K.M.; Hutson, P.H. The mGluR7 allosteric agonist AMN082 produces antidepressant-like effects by modulating glutamatergic signaling. Pharmacol. Biochem. Behav., 2012, 101(1), 35-40.
[] [PMID: 22138407]
O’Connor, R.M.; Cryan, J.F. The effects of mGlu7 receptor modulation in behavioural models sensitive to antidepressant action in two mouse strains. Behav. Pharmacol., 2013, 24(2), 105-113.
[] [PMID: 23455446]
Pałucha-Poniewiera, A.; Pilc, A. A selective mGlu7 receptor antagonist MMPIP reversed antidepressant-like effects of AMN082 in rats. Behav. Brain Res., 2013, 238, 109-112.
[] [PMID: 23085340]
Greco, B.; Lopez, S.; van der Putten, H.; Flor, P.J.; Amalric, M. Metabotropic glutamate 7 receptor subtype modulates motor symptoms in rodent models of Parkinson’s disease. J. Pharmacol. Exp. Ther., 2010, 332(3), 1064-1071.
[] [PMID: 19940105]
Konieczny, J.; Lenda, T. Contribution of the mGluR7 receptor to antiparkinsonian-like effects in rats: A behavioral study with the selective agonist AMN082. Pharmacol. Rep., 2013, 65(5), 1194-1203.
[] [PMID: 24399715]
Salling, M.C.; Faccidomo, S.; Hodge, C.W. Nonselective suppression of operant ethanol and sucrose self-administration by the mGluR7 positive allosteric modulator AMN082. Pharmacol. Biochem. Behav., 2008, 91(1), 14-20.
[] [PMID: 18593591]
Bahi, A. The pre-synaptic metabotropic glutamate receptor 7 “mGluR7” is a critical modulator of ethanol sensitivity in mice. Neuroscience, 2011, 199, 13-23.
[] [PMID: 22056957]
Li, X.; Li, J.; Peng, X.Q.; Spiller, K.; Gardner, E.L.; Xi, Z.X. Metabotropic glutamate receptor 7 modulates the rewarding effects of cocaine in rats: involvement of a ventral pallidal GABAergic mechanism. Neuropsychopharmacology, 2009, 34(7), 1783-1796.
[] [PMID: 19158667]
Li, X.; Xi, Z.X.; Markou, A. Metabotropic glutamate 7 (mGlu7) receptor: a target for medication development for the treatment of cocaine dependence. Neuropharmacology, 2013, 66, 12-23.
[] [PMID: 22546614]
Mares, P. AMN 082, an agonist of mGluR7, exhibits mixed anti- and proconvulsant effects in developing rats. Physiol. Res., 2008, 57(6), 969-972.
[PMID: 19154087]
Sukoff, R.S.J.; Leonard, S.K.; Gilbert, A.; Dollings, P.; Smith, D.L.; Zhang, M.Y.; Di, L.; Platt, B.J.; Neal, S.; Dwyer, J.M.; Bender, C.N.; Zhang, J.; Lock, T.; Kowal, D.; Kramer, A.; Randall, A.; Huselton, C.; Vishwanathan, K.; Tse, S.Y.; Butera, J.; Ring, R.H.; Rosenzweig-Lipson, S.; Hughes, Z.A.; Dunlop, J. The metabotropic glutamate receptor 7 allosteric modulator AMN082: a monoaminergic agent in disguise? J. Pharmacol. Exp. Ther., 2011, 338(1), 345-352.
[] [PMID: 21508084]
Ahnaou, A.; Raeyemaekers, L.; Huysmans, H.; Drinkenburg, W.H.I.M. Off-target potential of AMN082 on sleep EEG and related physiological variables: Evidence from mGluR7 (-/-) mice. Behav. Brain Res., 2016, 311, 287-297.
[] [PMID: 27211063]
Gee, C.E.; Peterlik, D.; Neuhäuser, C.; Bouhelal, R.; Kaupmann, K.; Laue, G.; Uschold-Schmidt, N.; Feuerbach, D.; Zimmermann, K.; Ofner, S.; Cryan, J.F.; van der Putten, H.; Fendt, M.; Vranesic, I.; Glatthar, R.; Flor, P.J. Blocking metabotropic glutamate receptor subtype 7 (mGlu7) via the Venus flytrap domain (VFTD) inhibits amygdala plasticity, stress, and anxiety-related behavior. J. Biol. Chem., 2014, 289(16), 10975-10987.
[] [PMID: 24596089]
Suzuki, G.; Tsukamoto, N.; Fushiki, H.; Kawagishi, A.; Nakamura, M.; Kurihara, H.; Mitsuya, M.; Ohkubo, M.; Ohta, H. In vitro pharmacological characterization of novel isoxazolopyridone derivatives as allosteric metabotropic glutamate receptor 7 antagonists. J. Pharmacol. Exp. Ther., 2007, 323(1), 147-156.
[] [PMID: 17609420]
Hikichi, H.; Murai, T.; Okuda, S.; Maehara, S.; Satow, A.
Ise, S.; Nishino, M.; Suzuki, G.; Takehana, H.; Hata, M.; Ohta, H. Effects of a novel metabotropic glutamate receptor 7 negative allosteric modulator, 6-(4-methoxyphenyl)-5-methyl-3-pyridin-4-ylisoxazonolo[4,5-c]pyridin-4(5H)-one (MMPIP), on the central nervous system in rodents. Eur. J. Pharmacol., 2010, 639(1-3), 106-114.
[] [PMID: 20371227]
Cieślik, P.; Woźniak, M.; Kaczorowska, K.; Brański, P.; Burnat, G.; Chocyk, A.; Bobula, B.; Gruca, P.; Litwa, E.; Pałucha-Poniewiera, A.; Wąsik, A.; Pilc, A.; Wierońska, J. Negative allosteric modulators of mGlu7 receptor as putative antipsychotic drugs. Front. Mol. Neurosci., 2018, 11, 316.
[] [PMID: 30294258]
Palazzo, E.; Romano, R.; Luongo, L.; Boccella, S.; De Gregorio, D.; Giordano, M.E.; Rossi, F.; Marabese, I.; Scafuro, M.A.; de Novellis, V.; Maione, S. MMPIP, an mGluR7-selective negative allosteric modulator, alleviates pain and normalizes affective and cognitive behavior in neuropathic mice. Pain, 2015, 156(6), 1060-1073.
[] [PMID: 25760470]
Kalinichev, M.; Rouillier, M.; Girard, F.; Royer-Urios, I.; Bournique, B.; Finn, T.; Charvin, D.; Campo, B.; Le Poul, E.; Mutel, V.; Poli, S.; Neale, S.A.; Salt, T.E.; Lütjens, R. ADX71743, a potent and selective negative allosteric modulator of metabotropic glutamate receptor 7: in vitro and in vivo characterization. J. Pharmacol. Exp. Ther., 2013, 344(3), 624-636.
[] [PMID: 23257312]
Pelkey, K.A.; Yuan, X.; Lavezzari, G.; Roche, K.W.; McBain, C.J. mGluR7 undergoes rapid internalization in response to activation by the allosteric agonist AMN082. Neuropharmacology, 2007, 52(1), 108-117.
[] [PMID: 16914173]
Gubellini, P.; Picconi, B.; Bari, M.; Battista, N.; Calabresi, P.; Centonze, D.; Bernardi, G.; Finazzi-Agrò, A.; Maccarrone, M. Experimental parkinsonism alters endocannabinoid degradation: implications for striatal glutamatergic transmission. J. Neurosci., 2002, 22(16), 6900-6907.
[] [PMID: 12177188]
Gubellini, P.; Pisani, A.; Centonze, D.; Bernardi, G.; Calabresi, P. Metabotropic glutamate receptors and striatal synaptic plasticity: implications for neurological diseases. Prog. Neurobiol., 2004, 74(5), 271-300.
[] [PMID: 15582223]
Hirsch, E.C.; Hunot, S.; Hartmann, A. Mechanism of cell death in experimental models of Parkinson’s disease. Funct. Neurol., 2000, 15(4), 229-237.
[PMID: 11213526]
Greenamyre, J.T. Glutamatergic influences on the basal ganglia. Clin. Neuropharmacol., 2001, 24(2), 65-70.
[] [PMID: 11307040]
Chase, T.N.; Bibbiani, F.; Oh, J.D. Striatal glutamatergic mechanisms and extrapyramidal movement disorders. Neurotox. Res., 2003, 5(1-2), 139-146.
[] [PMID: 12832228]
Carlsson, M.; Carlsson, A. Interactions between glutamatergic and monoaminergic systems within the basal ganglia--implications for schizophrenia and Parkinson’s disease. Trends Neurosci., 1990, 13(7), 272-276.
[] [PMID: 1695402]
Greenamyre, J.T.; O’Brien, C.F. N-methyl-D-aspartate antagonists in the treatment of Parkinson’s disease. Arch. Neurol., 1991, 48(9), 977-981.
[] [PMID: 1835370]
Blandini, F.; Nappi, G.; Tassorelli, C.; Martignoni, E. Functional changes of the basal ganglia circuitry in Parkinson’s disease. Prog. Neurobiol., 2000, 62(1), 63-88.
[] [PMID: 10821982]
Pisani, A.; Calabresi, P.; Centonze, D.; Bernardi, G. Activation of group III metabotropic glutamate receptors depresses glutamatergic transmission at corticostriatal synapse. Neuropharmacology, 1997, 36(6), 845-851.
[] [PMID: 9225312]
Bell, M.I.; Richardson, P.J.; Lee, K. Functional and molecular characterization of metabotropic glutamate receptors expressed in rat striatal cholinergic interneurones. J. Neurochem., 2002, 81(1), 142-149.
[] [PMID: 12067226]
Bonsi, P.; Cuomo, D.; Picconi, B.; Sciamanna, G.; Tscherter, A.; Tolu, M.; Bernardi, G.; Calabresi, P.; Pisani, A. Striatal metabotropic glutamate receptors as a target for pharmacotherapy in Parkinson’s disease. Amino Acids, 2007, 32(2), 189-195.
[] [PMID: 16715415]
Sebastianutto, I.; Cenci, M.A. mGlu receptors in the treatment of Parkinson’s disease and L-DOPA-induced dyskinesia. Curr. Opin. Pharmacol., 2018, 38, 81-89.
[] [PMID: 29625424]
Valenti, O.; Marino, M.J.; Conn, P.J. Modulation of excitatory transmission onto midbrain dopaminergic neurons of the rat by activation of group III metabotropic glutamate receptors. Ann. N. Y. Acad. Sci., 2003, 1003, 479-480.
[] [PMID: 14684494]
Konieczny, J.; Wardas, J.; Kuter, K.; Pilc, A.; Ossowska, K. The influence of group III metabotropic glutamate receptor stimulation by (1S,3R,4S)-1-aminocyclo-pentane-1,3,4-tricarboxylic acid on the parkinsonian-like akinesia and striatal proenkephalin and prodynorphin mRNA expression in rats. Neuroscience, 2007, 145(2), 611-620.
[] [PMID: 17224239]
Lopez, S.; Turle-Lorenzo, N.; Acher, F.; De Leonibus, E.; Mele, A.; Amalric, M. Targeting group III metabotropic glutamate receptors produces complex behavioral effects in rodent models of Parkinson’s disease. J. Neurosci., 2007, 27(25), 6701-6711.
[] [PMID: 17581957]
Sibille, P.; Lopez, S.; Brabet, I.; Valenti, O.; Oueslati, N.; Gaven, F.; Goudet, C.; Bertrand, H.O.; Neyton, J.; Marino, M.J.; Amalric, M.; Pin, J.P.; Acher, F.C. Synthesis and biological evaluation of 1-amino-2-phosphonomethylcyclopropanecarboxylic acids, new group III metabotropic glutamate receptor agonists. J. Med. Chem., 2007, 50(15), 3585-3595.
[] [PMID: 17602546]
Agari, T.; Yasuhara, T.; Matsui, T.; Kuramoto, S.; Kondo, A.; Miyoshi, Y.; Shingo, T.; Borlongan, C.V.; Date, I. Intrapallidal metabotropic glutamate receptor activation in a rat model of Parkinson’s disease: behavioral and histological analyses. Brain Res., 2008, 1203, 189-196.
[] [PMID: 18313647]
Conn, P.J.; Pin, J.P. Pharmacology and functions of metabotropic glutamate receptors. Annu. Rev. Pharmacol. Toxicol., 1997, 37, 205-237.
[] [PMID: 9131252]
G, S.; Suvarna, P.; Hadigal, S.; Kamath, P.; Prabhu, N.; Shenoy K, A.; Lc, P. Can metabotropic glutamate receptor 7 (mGluR 7) be a novel target for analgesia? J. Clin. Diagn. Res., 2014, 8(9), HC16-HC18.
[] [PMID: 25386457]
Osikowicz, M.; Skup, M.; Mika, J.; Makuch, W.; Czarkowska-Bauch, J.; Przewlocka, B. Glial inhibitors influence the mRNA and protein levels of mGlu2/3, 5 and 7 receptors and potentiate the analgesic effects of their ligands in a mouse model of neuropathic pain. Pain, 2009, 147(1-3), 175-186.
[] [PMID: 19782473]
Osikowicz, M.; Mika, J.; Makuch, W.; Przewlocka, B. Glutamate receptor ligands attenuate allodynia and hyperalgesia and potentiate morphine effects in a mouse model of neuropathic pain. Pain, 2008, 139(1), 117-126.
[] [PMID: 18442882]
Dolan, S.; Gunn, M.D.; Biddlestone, L.; Nolan, A.M. The selective metabotropic glutamate receptor 7 allosteric agonist AMN082 inhibits inflammatory pain-induced and incision-induced hypersensitivity in rat. Behav. Pharmacol., 2009, 20(7), 596-604.
[] [PMID: 19667973]
Dolan, S.; Gunn, M.D.; Crossan, C.; Nolan, A.M. Activation of metabotropic glutamate receptor 7 in spinal cord inhibits pain and hyperalgesia in a novel formalin model in sheep. Behav. Pharmacol., 2011, 22(5-6), 582-588.
[] [PMID: 21597362]
Marabese, I.; de Novellis, V.; Palazzo, E.; Scafuro, M.A.; Vita, D.; Rossi, F.; Maione, S. Effects of (S)-3,4-DCPG, an mGlu8 receptor agonist, on inflammatory and neuropathic pain in mice. Neuropharmacology, 2007, 52(2), 253-262. a.
[] [PMID: 17113112]
Marabese, I.; Rossi, F.; Palazzo, E.; de Novellis, V.; Starowicz, K.; Cristino, L.; Vita, D.; Gatta, L.; Guida, F.; Di Marzo, V.; Rossi, F.; Maione, S. Periaqueductal gray metabotropic glutamate receptor subtype 7 and 8 mediate opposite effects on amino acid release, rostral ventromedial medulla cell activities, and thermal nociception. J. Neurophysiol., 2007, 98(1), 43-53. b.
[] [PMID: 17507496]
Heinricher, M.M.; Tortorici, V. Interference with GABA transmission in the rostral ventromedial medulla: disinhibition of off-cells as a central mechanism in nociceptive modulation. Neuroscience, 1994, 63(2), 533-546.
[] [PMID: 7891863]
Palazzo, E.; Fu, Y.; Ji, G.; Maione, S.; Neugebauer, V. Group III mGluR7 and mGluR8 in the amygdala differentially modulate nocifensive and affective pain behaviors. Neuropharmacology, 2008, 55(4), 537-545.
[] [PMID: 18533199]
Pereira, V.; Goudet, C. Emerging trends in pain modulation by metabotropic glutamate receptors. Front. Mol. Neurosci., 2019, 11, 464.
[] [PMID: 30662395]
Palazzo, E.; Marabese, I.; Soukupova, M.; Luongo, L.; Boccella, S.; Giordano, C.; de Novellis, V.; Rossi, F.; Maione, S. Metabotropic glutamate receptor subtype 8 in the amygdala modulates thermal threshold, neurotransmitter release, and rostral ventromedial medulla cell activity in inflammatory pain. J. Neurosci., 2011, 31(12), 4687-4697.
[] [PMID: 21430167]
Palazzo, E.; de Novellis, V.; Rossi, F.; Maione, S. Supraspinal metabotropic glutamate receptor subtype 8: a switch to turn off pain. Amino Acids, 2014, 46(6), 1441-1448. a.
[] [PMID: 24623118]
Palazzo, E.; Marabese, I.; de Novellis, V.; Rossi, F.; Maione, S. Supraspinal metabotropic glutamate receptors: A target for pain relief and beyond. Eur. J. Neurosci., 2014, 39(3), 444-454. b.
[] [PMID: 24494684]
Palazzo, E.; Marabese, I.; de Novellis, V.; Rossi, F.; Maione, S. Metabotropic glutamate receptor 7: From synaptic function to therapeutic implications. Curr. Neuropharmacol., 2016, 14(5), 504-513.
[] [PMID: 27306064]
Palazzo, E.; Marabese, I.; Luongo, L.; Guida, F.; de Novellis, V.; Maione, S. Nociception modulation by supraspinal group III metabotropic glutamate receptors. J. Neurochem., 2017, 141(4), 507-519.
[] [PMID: 27363363]
Liu, X.H.; Han, M.; Zhu, J.X.; Sun, N.; Tang, J.S.; Huo, F.Q.; Li, J.; Xu, F.Y.; Du, J.Q. Metabotropic glutamate subtype 7 and 8 receptors oppositely modulate cardiac nociception in the rat nucleus tractus solitarius. Neuroscience, 2012, 220, 322-329.
[] [PMID: 22617702]
Kahl, E.; Fendt, M. Metabotropic glutamate receptors 7 within the nucleus accumbens are involved in relief learning in rats. Curr. Neuropharmacol., 2016, 14(5), 405-412.
[] [PMID: 27296637]
Moloney, R.D.; Golubeva, A.V.; O’Connor, R.M.; Kalinichev, M.; Dinan, T.G.; Cryan, J.F. Negative allosteric modulation of the mGlu7 receptor reduces visceral hypersensitivity in a stress-sensitive rat strain. Neurobiol. Stress, 2015, 2, 28-33.
[] [PMID: 26844237]
Palazzo, E.; Marabese, I.; Luongo, L.; Boccella, S.; Bellini, G.; Giordano, M.E.; Rossi, F.; Scafuro, M.; Novellis, Vd.; Maione, S. Effects of a metabotropic glutamate receptor subtype 7 negative allosteric modulator in the periaqueductal grey on pain responses and rostral ventromedial medulla cell activity in rat. Mol. Pain, 2013, 9, 44.
[] [PMID: 24004843]
Wei, X.; Yang, D.; Shi, T.; Wang, J.; Deng, Y.; Qiao, X.; Yang, C.; Xu, M. Metabotropic glutamate receptor 7 (mGluR7) as a target for modulating pain-evoked activities of neurons in the hippocampal CA3 region of rats. CNS Neurol. Disord. Drug Targets, 2017, 16(5), 610-616.
[] [PMID: 27488423]
Ansah, O.B.; Leite-Almeida, H.; Wei, H.; Pertovaara, A. Striatal dopamine D2 receptors attenuate neuropathic hypersensitivity in the rat. Exp. Neurol., 2007, 205, 536-546.
Malherbe, P.; Kratzeisen, C.; Lundstrom, K.; Richards, J.G.; Faull, R.L.; Mutel, V. Cloning and functional expression of alternative spliced variants of the human metabotropic glutamate receptor 8. Brain Res. Mol. Brain Res., 1999, 67(2), 201-210.
[] [PMID: 10216218]
Kinoshita, A.; Ohishi, H.; Nomura, S.; Shigemoto, R.; Nakanishi, S.; Mizuno, N. Presynaptic localization of a metabotropic glutamate receptor, mGluR4a, in the cerebellar cortex: a light and electron microscope study in the rat. Neurosci. Lett., 1996, 207(3), 199-202.
[] [PMID: 8728484]
Shigemoto, R.; Kinoshita, A.; Wada, E.; Nomura, S.; Ohishi, H.; Takada, M.; Flor, P.J.; Neki, A.; Abe, T.; Nakanishi, S.; Mizuno, N. Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J. Neurosci., 1997, 17(19), 7503-7522.
[] [PMID: 9295396]
Ferraguti, F.; Klausberger, T.; Cobden, P.; Baude, A.; Roberts, J.D.; Szucs, P.; Kinoshita, A.; Shigemoto, R.; Somogyi, P.; Dalezios, Y. Metabotropic glutamate receptor 8-expressing nerve terminals target subsets of GABAergic neurons in the hippocampus. J. Neurosci., 2005, 25(45), 10520-10536.
[] [PMID: 16280590]
Catania, M.V.; De Socarraz, H.; Penney, J.B.; Young, A.B. Metabotropic glutamate receptor heterogeneity in rat brain. Mol. Pharmacol., 1994, 45(4), 626-636.
[PMID: 8183241]
Saugstad, J.A.; Kinzie, J.M.; Shinohara, M.M.; Segerson, T.P.; Westbrook, G.L. Cloning and expression of rat metabotropic glutamate receptor 8 reveals a distinct pharmacological profile. Mol. Pharmacol., 1997, 51(1), 119-125.
[] [PMID: 9016353]
Koulen, P.; Kuhn, R.; Wässle, H.; Brandstätter, J.H. Modulation of the intracellular calcium concentration in photoreceptor terminals by a presynaptic metabotropic glutamate receptor. Proc. Natl. Acad. Sci. USA, 1999, 96(17), 9909-9914.
[] [PMID: 10449793]
Robbins, M.J.; Starr, K.R.; Honey, A.; Soffin, E.M.; Rourke, C.; Jones, G.A.; Kelly, F.M.; Strum, J.; Melarange, R.A.; Harris, A.J.; Rocheville, M.; Rupniak, T.; Murdock, P.R.; Jones, D.N.; Kew, J.N.; Maycox, P.R. Evaluation of the mGlu8 receptor as a putative therapeutic target in schizophrenia. Brain Res., 2007, 1152, 215-227.
[] [PMID: 17434465]
Thomas, N.K.; Wright, R.A.; Howson, P.A.; Kingston, A.E.; Schoepp, D.D.; Jane, D.E. (S)-3,4-DCPG, a potent and selective mGlu8a receptor agonist, activates metabotropic glutamate receptors on primary afferent terminals in the neonatal rat spinal cord. Neuropharmacology, 2001, 40(3), 311-318.
[] [PMID: 11166323]
Tong, Q.; Ouedraogo, R.; Kirchgessner, A.L. Localization and function of group III metabotropic glutamate receptors in rat pancreatic islets. Am. J. Physiol. Endocrinol. Metab., 2002, 282(6), E1324-E1333.
[] [PMID: 12006363]
Tong, Q.; Kirchgessner, A.L. Localization and function of metabotropic glutamate receptor 8 in the enteric nervous system. Am. J. Physiol. Gastrointest. Liver Physiol., 2003, 285(5), G992-G1003.
[] [PMID: 12829438]
Schoepp, D.D. Unveiling the functions of presynaptic metabotropic glutamate receptors in the central nervous system. J. Pharmacol. Exp. Ther., 2001, 299(1), 12-20.
[PMID: 11561058]
Gerlai, R.; Adams, B.; Fitch, T.; Chaney, S.; Baez, M. Performance deficits of mGluR8 knockout mice in learning tasks: the effects of null mutation and the background genotype. Neuropharmacology, 2002, 43(2), 235-249.
[] [PMID: 12213278]
Linden, A.M.; Johnson, B.G.; Peters, S.C.; Shannon, H.E.; Tian, M.; Wang, Y.; Yu, J.L.; Köster, A.; Baez, M.; Schoepp, D.D. Increased anxiety-related behavior in mice deficient for metabotropic glutamate 8 (mGlu8) receptor. Neuropharmacology, 2002, 43(2), 251-259.
[] [PMID: 12213279]
Linden, A.M.; Baez, M.; Bergeron, M.; Schoepp, D.D. Increased c-Fos expression in the centromedial nucleus of the thalamus in metabotropic glutamate 8 receptor knockout mice following the elevated plus maze test. Neuroscience, 2003, 121(1), 167-178.
[] [PMID: 12946709]
Duvoisin, R.M.; Pfankuch, T.; Wilson, J.M.; Grabell, J.; Chhajlani, V.; Brown, D.G.; Johnson, E.; Raber, J. Acute pharmacological modulation of mGluR8 reduces measures of anxiety. Behav. Brain Res., 2010, 212(2), 168-173.
[] [PMID: 20385173]
Duvoisin, R.M.; Villasana, L.; Pfankuch, T.; Raber, J. Sex-dependent cognitive phenotype of mice lacking mGluR8. Behav. Brain Res., 2010, 209(1), 21-26.
[] [PMID: 20080129]
Fendt, M.; Bürki, H.; Imobersteg, S.; van der Putten, H.; McAllister, K.; Leslie, J.C.; Shaw, D.; Hölscher, C. The effect of mGlu8 deficiency in animal models of psychiatric diseases. Genes Brain Behav., 2010, 9(1), 33-44.
[] [PMID: 19740090]
Duvoisin, R.M.; Zhang, C.; Pfankuch, T.F.; O’Connor, H.; Gayet-Primo, J.; Quraishi, S.; Raber, J. Increased measures of anxiety and weight gain in mice lacking the group III metabotropic glutamate receptor mGluR8. Eur. J. Neurosci., 2005, 22(2), 425-436.
[] [PMID: 16045496]
Raber, J.; Duvoisin, R.M. Novel metabotropic glutamate receptor 4 and glutamate receptor 8 therapeutics for the treatment of anxiety. Expert Opin. Investig. Drugs, 2015, 24(4), 519-528.
[] [PMID: 25518990]
Torres, E.R.S.; Akinyeke, T.; Stagaman, K.; Duvoisin, R.M.; Meshul, C.K.; Sharpton, T.J.; Raber, J. Effects of sub-chronic MPTP exposure on behavioral and cognitive performance and the microbiome of wild-type and mGlu8 knockout female and male mice. Front. Behav. Neurosci., 2018, 12, 140.
[] [PMID: 30072879]
Crawley, J.N. Behavioral phenotyping of transgenic and knockout mice: experimental design and evaluation of general health, sensory functions, motor abilities, and specific behavioral tests. Brain Res., 1999, 835(1), 18-26.
[] [PMID: 10448192]
Cryan, J.F.; Holmes, A. The ascent of mouse: advances in modelling human depression and anxiety. Nat. Rev. Drug Discov., 2005, 4(9), 775-790.
[] [PMID: 16138108]
Moldrich, R.X.; Beart, P.M.; Jane, D.E.; Chapman, A.G.; Meldrum, B.S. Anticonvulsant activity of 3,4-dicarboxyphenylglycines in DBA/2 mice. Neuropharmacology, 2001, 40(5), 732-735.
[] [PMID: 11311902]
Lee, J.J.; Jane, D.E.; Croucher, M.J. Anticonvulsant dicarboxyphenylglycines differentially modulate excitatory amino acid release in the rat cerebral cortex. Brain Res., 2003, 977(1), 119-123.
[] [PMID: 12788521]
Jiang, F.L.; Tang, Y.C.; Chia, S.C.; Jay, T.M.; Tang, F.R. Anticonvulsive effect of a selective mGluR8 agonist (S)-3,4-dicarboxyphenylglycine (S-3,4-DCPG) in the mouse pilocarpine model of status epilepticus. Epilepsia, 2007, 48(4), 783-792.
[] [PMID: 17430409]
Folbergrová, J.; Druga, R.; Haugvicová, R.; Mares, P.; Otáhal, J. Anticonvulsant and neuroprotective effect of (S)-3,4-dicarbo-xyphenylglycine against seizures induced in immature rats by homocysteic acid. Neuropharmacology, 2008, 54(4), 665-675.
[] [PMID: 18191956]
Bäckström, P.; Hyytiä, P. Suppression of alcohol self-administration and cue-induced reinstatement of alcohol seeking by the mGlu2/3 receptor agonist LY379268 and the mGlu8 receptor agonist (S)-3,4-DCPG. Eur. J. Pharmacol., 2005, 528(1-3), 110-118.
[] [PMID: 16324694]
Bahi, A. Decreased anxiety, voluntary ethanol intake and ethanol-induced CPP acquisition following activation of the metabotropic glutamate receptor 8 “mGluR8”. Pharmacol. Biochem. Behav., 2017, 155, 32-42.
Schmid, S.; Fendt, M. Effects of the mGluR8 agonist (S)-3,4-DCPG in the lateral amygdala on acquisition/expression of fear-potentiated startle, synaptic transmission, and plasticity. Neuropharmacology, 2006, 50(2), 154-164.
[]] [PMID: 16188284]
Dobi, A.; Sartori, S.B.; Busti, D.; Van der Putten, H.; Singewald, N.; Shigemoto, R.; Ferraguti, F. Neural substrates for the distinct effects of presynaptic group III metabotropic glutamate receptors on extinction of contextual fear conditioning in mice. Neuropharmacology, 2013, 66, 274-289.
[] [PMID: 22643400]
Johnson, K.A.; Jones, C.K.; Tantawy, M.N.; Bubser, M.; Marvanova, M.; Ansari, M.S.; Baldwin, R.M.; Conn, P.J.; Niswender, C.M. The metabotropic glutamate receptor 8 agonist (S)-3,4-DCPG reverses motor deficits in prolonged but not acute models of Parkinson’s disease. Neuropharmacology, 2013, 66, 187-195.
[] [PMID: 22546615]
Mercier, M.S.; Lodge, D.; Fang, G.; Nicolas, C.S.; Collett, V.J.; Jane, D.E.; Collingridge, G.L.; Bortolotto, Z.A. Characterisation of an mGlu8 receptor-selective agonist and antagonist in the lateral and medial perforant path inputs to the dentate gyrus. Neuropharmacology, 2013, 67, 294-303.
[] [PMID: 23220400]
Ossowska, K.; Pietraszek, M.; Wardas, J.; Wolfarth, S. Potential antipsychotic and extrapyramidal effects of (R,S)-3,4-dicarboxyphenylglycine [(R,S)-3,4-DCPG], a mixed AMPA antagonist/mGluR8 agonist. Pol. J. Pharmacol., 2004, 56(3), 295-304.
[PMID: 15215559]
Maj, J.; Rogóz, Z.; Skuza, G.; Jaros, T. Some behavioral effects of CNQX AND NBQX, AMPA receptor antagonists. Pol. J. Pharmacol., 1995, 47(4), 269-277.
[PMID: 8616504]
Beckstead, R.M. N-methyl-D-aspartate acutely increases proenkephalin mRNA in the rat striatum. Synapse, 1995, 21(4), 342-347.
[] [PMID: 8869164]
Mörl, F.; Gröschel, M.; Leemhuis, J.; Meyer, D.K. Intrinsic GABA neurons inhibit proenkephalin gene expression in slice cultures of rat neostriatum. Eur. J. Neurosci., 2002, 15(7), 1115-1124.
[] [PMID: 11982623]
Marabese, I.; de Novellis, V.; Palazzo, E.; Mariani, L.; Siniscalco, D.; Rodella, L.; Rossi, F.; Maione, S. Differential roles of mGlu8 receptors in the regulation of glutamate and gamma-aminobutyric acid release at periaqueductal grey level. Neuropharmacology, 2005, 49(Suppl. 1), 157-166.
[] [PMID: 16084932]
Menétrey, D.; Basbaum, A.I. Spinal and trigeminal projections to the nucleus of the solitary tract: a possible substrate for somatovisceral and viscerovisceral reflex activation. J. Comp. Neurol., 1987, 255(3), 439-450.
[] [PMID: 3819024]
Reynolds, D.V. Surgery in the rat during electrical analgesia induced by focal brain stimulation. Science, 1969, 164(3878), 444-445.
[] [PMID: 4887743]
Helmstetter, F.J. The amygdala is essential for the expression of conditional hypoalgesia. Behav. Neurosci., 1992, 106(3), 518-528.
[] [PMID: 1319714]
Helmstetter, F.J.; Bellgowan, P.S. Lesions of the amygdala block conditional hypoalgesia on the tail flick test. Brain Res., 1993, 612(1-2), 253-257.
[] [PMID: 8330203]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy