Pharmacological enhancement of mGlu1 metabotropic glutamate receptors causes a prolonged symptomatic benefit in a mouse model of spinocerebellar ataxia type 1

Molecular Brain

Volumn 6, Issue 1, 2013, Pages

  Notartomaso, Serena ^a   Zappulla, Cristina ^a   Biagioni, Francesca ^a   Cannella, Milena ^a   Bucci, Domenico ^a   Mascio, Giada ^a   Scarselli, Pamela ^a   Fazio, Francesco ^a   Weisz, Filippo ^b   Lionetto, Luana ^c   Simmaco, Maurizio ^c   Gradini, Roberto ^a,d   Battaglia, Giuseppe ^a   Signore, Michele ^e   Puliti, Aldamaria ^f   Nicoletti, Ferdinando ^a,b  

^a IRCCS NEUROMED   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

^e ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^f G GASLINI INSTITUTE   (Italy)

Author keywords

JNJ16259685; mGlu1 receptor; mGlu5 receptor; Motor coordination; Purkinje cell; Ro0711401; Spinocerebellar ataxia type 1; VU0360172

Indexed keywords

AMPA RECEPTOR; JNJ 16259685; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR 5; METABOTROPIC RECEPTOR AGONIST; METABOTROPIC RECEPTOR ANTAGONIST; RO 0711401; UNCLASSIFIED DRUG; VU 0360172;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL SIZE; CEREBELLUM; CONTROLLED STUDY; DENDRITIC SPINE; DRUG CLEARANCE; MOTOR PERFORMANCE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PURKINJE CELL; SPINOCEREBELLAR ATAXIA TYPE 1; SPINOCEREBELLAR DEGENERATION; SYSTEMIC THERAPY; TREATMENT RESPONSE;

MUS; MUS MUSCULUS;

AMIDES; ANIMALS; CEREBELLUM; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; MASS SPECTROMETRY; MICE; MOTOR ACTIVITY; NIACINAMIDE; PURKINJE CELLS; RECEPTOR, METABOTROPIC GLUTAMATE 5; RECEPTORS, METABOTROPIC GLUTAMATE; RNA, MESSENGER; SPINOCEREBELLAR ATAXIAS;

EID: 84887750408     PISSN: None     EISSN: 17566606     Source Type: Journal    
DOI: 10.1186/1756-6606-6-48     Document Type: Article

References (63)

1. Expansion of an unstable trinucleotide CAG repeat in spinocerebellar ataxia type 1. Orr HT, Chung MY, Banfi S, Kwiatkowski TJ Jr, Servadio A, Beaudet AL, McCall AE, Duvick LA, Ranum LP, Zoghbi HY, Nat Genet 1993 4 221 226 10.1038/ng0793-221 8358429 (Pubitemid 23205168)
2. The pathogenesis of spinocerebellar ataxia. Koeppen AH, Cerebellum 2005 4 62 73 10.1080/14734220510007950 15895563 (Pubitemid 40592813)
3. A long CAG repeat in the mouse Sca1 locus replicates SCA1 features and reveals the impact of protein solubility on selective neurodegeneration. Watase K, Weeber EJ, Xu B, Antalffy B, Yuva-Paylor L, Hashimoto K, Kano M, Atkinson R, Sun Y, Armstrong DL, Sweatt JD, Orr HT, Paylor R, Zoghbi HY, Neuron 2002 34 905 919 10.1016/S0896-6273(02)00733-X 12086639 (Pubitemid 34722281)
4. The unstable repeats-three evolving faces of neurological disease. Nelson DL, Orr HT, Warren ST, Neuron 2013 77 825 843 10.1016/j.neuron.2013.02.022 23473314
5. Metabotropic glutamate receptors: from the workbench to the bedside. Nicoletti F, Bockaert J, Collingridge GL, Conn PJ, Ferraguti F, Schoepp DD, Wroblewski JT, Pin JP, Neuropharmacology 2011 60 1017 1041 10.1016/j.neuropharm. 2010.10.022 21036182
6. Glutamate receptors: brain function and signal transduction. Nakanishi S, Nakajima Y, Masu M, Ueda Y, Nakahara K, Watanabe D, Yamaguchi S, Kawabata S, Okada M, Brain Res Rev 1998 26 230 235 10.1016/S0165-0173(97)00033-7 9651535 (Pubitemid 28318078)
7. The metabotropic glutamate receptor (mGluR1 alpha) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Baude A, Nusser Z, Roberts JD, Mulvihill E, McIlhinney RA, Somogyi P, Neuron 1993 11 771 787 10.1016/0896-6273(93)90086-7 8104433 (Pubitemid 23321784)
8. Metabotropic glutamate 1 receptor: current concepts and perspectives. Ferraguti F, Crepaldi L, Nicoletti F, Pharmacol Rev 2008 60 536 581 10.1124/pr.108.000166 19112153
9. Expression and coupling to polyphosphoinositide hydrolysis of group I metabotropic glutamate receptors in early postnatal and adult rat brain. Casabona G, Knöpfel T, Kuhn R, Gasparini F, Baumann P, Sortino MA, Copani A, Nicoletti F, Eur J Neurosci 1997 9 12 17 10.1111/j.1460-9568.1997.tb01348.x 9042564 (Pubitemid 27083470)
10. Induction of long-term depression in cerebellar Purkinje cells requires a rapidly turned over protein. Karachot L, Shirai Y, Vigot R, Yamamori T, Ito M, J Neurophysiol 2001 86 280 289 11431509 (Pubitemid 32623233)
11. mGluR1 in cerebellar Purkinje cells essential for long-term depression, synapse elimination, and motor coordination. Ichise T, Kano M, Hashimoto K, Yanagihara D, Nakao K, Shigemoto R, Katsuki M, Aiba A, Science 2000 288 1832 1835 10.1126/science.288.5472.1832 10846166 (Pubitemid 30399022)
12. Long-term depression of the cerebellar climbing fiber-Purkinje neuron synapse. Hansel C, Linden DJ, Neuron 2000 26 473 482 10.1016/S0896-6273(00) 81179-4 10839365
13. Participation of postsynaptic PKC in cerebellar long-term depression in culture. Linden DJ, Connor JA, Science 1991 254 1656 1659 10.1126/science. 1721243 1721243 (Pubitemid 21917512)
14. Synaptic mechanisms of the cerebellar cortical network. Nakanishi S, Trends Neurosci 2005 28 93 100 10.1016/j.tins.2004.12.004 15667932 (Pubitemid 40178926)
15. Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice. Aiba A, Kano M, Chen C, Stanton ME, Fox GD, Herrup K, Zwingman TA, Tonegawa S, Cell 1994 79 377 388 10.1016/0092-8674(94)90205-4 7954803 (Pubitemid 24324926)
16. Motor deficit and impairment of synaptic plasticity in mice lacking mGluR1. Conquet F, Bashir ZI, Davies HC, Daniel H, Ferraguti F, Bordi F, Franz-Bacon K, Reggiani A, Matarese V, Condé F, Collingridge GL, Crépe LF, Nature 1994 372 237 243 10.1038/372237a0 7969468 (Pubitemid 24352443)
17. Crv4, a mouse model for human ataxia associated with kyphoscoliosis caused by an mRNA splicing mutation of the metabotropic glutamate receptor 1 (Grm1). Conti V, Aghaie A, Cilli M, Martin N, Caridi G, Musante L, Candiano G, Castagna M, Fairen A, Ravazzolo R, Guenet JL, Puliti A, Int J Mol Med 2006 18 593 600 16964410
18. mGluR1 in cerebellar Purkinje cells is required for normal association of temporally contiguous stimuli in classical conditioning. Kishimoto Y, Fujimichi R, Araishi K, Kawahara S, Kano M, Aiba A, Kirino Y, Eur J Neurosci 2002 16 2416 2424 10.1046/j.1460-9568.2002.02407.x 12492436 (Pubitemid 36056965)
19. The mouse mutants recoil wobbler and nmf373 represent a series of Grm1 mutations. Sachs AJ, Schwendinger JK, Yang AW, Haider NB, Nystuen AM, Mamm Genome 2007 18 749 756 10.1007/s00335-007-9064-y 17934773 (Pubitemid 350160086)
20. Molecular alterations in the cerebellum of the plasma membrane calcium ATPase 2 (PMCA2)-null mouse indicate abnormalities in Purkinje neurons. Kurnellas MP, Lee AK, Li H, Deng L, Ehrlich DJ, Elkabes S, Mol Cell Neurosci 2007 34 178 188 10.1016/j.mcn.2006.10.010 17150372 (Pubitemid 46157105)
21. Disruption of metabotropic glutamate receptor signalling is a major defect at cerebellar parallel fibre-Purkinje cell synapses in staggerer mutant mice. Mitsumura K, Hosoi N, Furuya N, Hirai H, J Physiol 2011 589 3191 3209 10.1113/jphysiol.2011.207563 21558162
22. Paraneoplastic cerebellar ataxia due to autoantibodies against a glutamate receptor. Sillevis Smitt P, Kinoshita A, De Leeuw B, Moll W, Coesmans M, Jaarsma D, Henzen-Logmans S, Vecht C, De Zeeuw C, Sekiyama N, Nakanishi S, Shigemoto R, N Engl J Med 2000 342 21 27 10.1056/NEJM200001063420104 10620645 (Pubitemid 30020656)
23. Altered trafficking of membrane proteins in purkinje cells of SCA1 transgenic mice. Skinner PJ, Vierra-Green CA, Clark HB, Zoghbi HY, Orr HT, Am J Pathol 2001 159 905 913 10.1016/S0002-9440(10)61766-X 11549583 (Pubitemid 32847181)
24. Recovery from polyglutamine-induced neurodegeneration in conditional SCA1 transgenic mice. Zu T, Duvick LA, Kaytor MD, Berlinger MS, Zoghbi HY, Clark HB, Orr HT, J Neurosci 2004 24 8853 8861 10.1523/JNEUROSCI.2978-04.2004 15470152 (Pubitemid 39362981)
25. Polyglutamine expansion down-regulates specific neuronal genes before pathologic changes in SCA1. Lin X, Antalffy B, Kang D, Orr HT, Zoghbi HY, Nat Neurosci 2000 3 157 163 10.1038/72101 10649571 (Pubitemid 30126331)
26. Gene profiling links SCA1 pathophysiology to glutamate signaling in Purkinje cells of transgenic mice. Serra HG, Byam CE, Lande JD, Tousey SK, Zoghbi HY, Orr HT, Hum Mol Genet 2004 13 2535 2543 10.1093/hmg/ddh268 15317756 (Pubitemid 39377856)
27. Allosteric modulation of metabotropic glutamate receptors. Sheffler DJ, Gregory KJ, Rook JM, Conn PJ, Adv Pharmacol 2011 62 37 77 21907906
28. "Molecular switches" on mGluR allosteric ligands that modulate modes of pharmacology. Wood MR, Hopkins CR, Brogan JT, Conn PJ, Lindsley CW, Biochemistry 2011 50 2403 2410 10.1021/bi200129s 21341760
29. Allosteric modulation of metabotropic glutamate receptors: structural insights and therapeutic potential. Gregory KJ, Dong EN, Meiler J, Conn PJ, Neuropharmacology 2011 60 66 81 10.1016/j.neuropharm.2010.07.007 20637216
30. Persistent multiple climbing fiber innervation of cerebellar Purkinje cells in mice lacking mGluR1. Kano M, Hashimoto K, Kurihara H, Watanabe M, Inoue Y, Aiba A, Tonegawa S, Neuron 1997 18 1 71 79 10.1016/S0896-6273(01)80047-7 9010206 (Pubitemid 27053831)
31. Purkinje cell ataxin-1 modulates climbing fiber synaptic input in developing and adult mouse cerebellum. Ebner BA, Ingram MA, Barnes JA, Duvick LA, Frisch JL, Clark HB, Zoghbi HY, Ebner TJ, Orr HT, J Neurosci 2013 33 13 5806 5820 27 10.1523/JNEUROSCI.6311-11.2013 23536093
32. Disruption of AMPA receptor GluR2 clusters following long-term depression induction in cerebellar Purkinje neurons. Matsuda S, Launey T, Mikawa S, Hirai H, EMBO J 2000 19 2765 2774 10.1093/emboj/19.12.2765 10856222 (Pubitemid 30386749)
33. Requirement of AMPA receptor GluR2 phosphorylation for cerebellar long-term depression. Chung HJ, Steinberg JP, Huganir RL, Linden DJ, Science 2003 300 1751 1755 10.1126/science.1082915 12805550 (Pubitemid 36712572)
34. N-ethylmaleimide-sensitive factor is required for the synaptic incorporation and removal of AMPA receptors during cerebellar long-term depression. Steinberg JP, Huganir RL, Linden DJ, Proc Natl Acad Sci USA 2004 101 18212 18216 10.1073/pnas.0408278102 15608060 (Pubitemid 40054099)
35. Targeted in vivo mutations of the AMPA receptor subunit GluR2 and its interacting protein PICK1 eliminate cerebellar long-term depression. Steinberg JP, Takamiya K, Shen Y, Xia J, Rubio ME, Yu S, Jin W, Thomas GM, Linden DJ, Huganir RL, Neuron 2006 49 845 860 10.1016/j.neuron.2006.02.025 16543133 (Pubitemid 43376082)
36. Involvement of basal protein kinase C and extracellular signal-regulated kinase 1/2 activities in constitutive internalization of AMPA receptors in cerebellar Purkinje cells. Tatsukawa T, Chimura T, Miyakawa H, Yamaguchi K, J Neurosci 2006 26 4820 4825 10.1523/JNEUROSCI.0535-06.2006 16672655 (Pubitemid 44315322)
37. The glutamate receptor-interacting protein family of GluR2-binding proteins is required for long-term synaptic depression expression in cerebellar Purkinje cells. Takamiya K, Mao L, Huganir RL, Linden DJ, J Neurosci 2008 28 5752 5755 10.1523/JNEUROSCI.0654-08.2008 18509036
38. Metabotropic glutamate receptors are differentially regulated during development. Catania MV, Landwehrmeyer GB, Testa CM, Standaert DG, Penney JB Jr, Young AB, Neuroscience 1994 61 481 495 10.1016/0306-4522(94)90428-6 7969925 (Pubitemid 24240298)
39. Switch in the expression of mGlu1 and mGlu5 metabotropic glutamate receptors in the cerebellum of mice developing experimental autoimmune encephalomyelitis and in autoptic cerebellar samples from patients with multiple sclerosis. Fazio F, Notartomaso S, Aronica E, Storto M, Battaglia G, Vieira E, Gatti S, Bruno V, Biagioni F, Gradini R, Nicoletti F, Di Marco R, Neuropharmacology 2008 55 491 499 10.1016/j.neuropharm.2008.06.066 18619983
40. Control of calcium oscillations by phosphorylation of metabotropic glutamate receptors. Kawabata S, Tsutsumi R, Kohara A, Yamaguchi T, Nakanishi S, Okada M, Nature 1996 383 89 92 10.1038/383089a0 8779726 (Pubitemid 26296467)
41. Cytosolic calcium oscillators. Berridge MJ, Galione A, FASEB J 1988 2 3074 3082 2847949
42. Calcium signalling: dynamics, homeostasis and remodelling. Berridge MJ, Bootman MD, Roderick HL, Nat Rev Mol Cell Biol 2003 4 517 529 10.1038/nrm1155 12838335 (Pubitemid 36773404)
43. Discovery of novel allosteric modulators of metabotropic glutamate receptor subtype 5 reveals chemical and functional diversity and in vivo activity in rat behavioral models of anxiolytic and antipsychotic activity. Rodriguez AL, Grier MD, Jones CK, Herman EJ, Kane AS, Smith RL, Williams R, Zhou Y, Marlo JE, Days EL, Blatt TN, Jadhav S, Menon UN, Vinson PN, Rook JM, Stauffer SR, Niswender CM, Lindsley CW, Weaver CD, Conn PJ, Mol Pharmacol 2010 78 1105 1123 10.1124/mol.110.067207 20923853
44. Potentiation of mGlu5 receptors with the novel enhancer, VU0360172, reduces spontaneous absence seizures in WAG/Rij rats. D'Amore V, Santolini I, van Rijn CM, Biagioni F, Molinaro G, Prete A, Conn PJ, Lindsley CW, Zhou Y, Vinson PN, Rodriguez AL, Jones CK, Stauffer SR, Nicoletti F, van Luijtelaar G, Ngomba RT, Neuropharmacology 2013 66 330 338 22705340
45. Fluorinated: 9H-xanthene-9-carboxylic acid oxazol-2-yl-amides as potent, orally available mGlu1 receptor enhancers. Vieira E, Huwyler J, Jolidon S, Knoflach F, Mutel V, Wichmann J, Bioorg Med Chem Lett 2009 19 1666 1669 10.1016/j.bmcl.2009.01.108 19233648
46. Protective role for type-1 metabotropic glutamate receptors against spike and wave discharges in the WAG/Rij rat model of absence epilepsy. Ngomba RT, Santolini I, Biagioni F, Molinaro G, Simonyi A, van Rijn CM, D'Amore V, Mastroiacovo F, Olivieri G, Gradini R, Ferraguti F, Battaglia G, Bruno V, Puliti A, van Luijtelaar G, Nicoletti F, Neuropharmacology 2011 60 1281 1291 10.1016/j.neuropharm.2011.01.007 21277877
47. Memory trace of motor learning shifts transsynaptically from cerebellar cortex to nuclei for consolidation. Shutoh F, Ohki M, Kitazawa H, Itohara S, Nagao S, Neuroscience 2006 139 2 767 777 10.1016/j.neuroscience.2005.12.035 16458438
48. Expression of cerebellar long-term depression requires postsynaptic clathrin-mediated endocytosis. Wang YT, Linden DJ, Neuron 2000 25 635 647 10.1016/S0896-6273(00)81066-1 10774731
49. Type-1 metabotropic glutamate receptor in cerebellar Purkinje cells: a key molecule responsible for long-term depression, endocannabinoid signalling and synapse elimination. Kano M, Hashimoto K, Tabata T, Philos Trans R Soc Lond B Biol Sci 2008 363 2173 2186 10.1098/rstb.2008.2270 18339599 (Pubitemid 351693529)
50. Cytoplasmic polyadenylation element binding protein 1-mediated mRNA translation in Purkinje neurons is required for cerebellar long-term depression and motor coordination. McEvoy M, Cao G, Montero Llopis P, Kundel M, Jones K, Hofler C, Shin C, Wells DG, J Neurosci 2007 27 6400 6411 10.1523/JNEUROSCI.5211- 06.2007 17567800 (Pubitemid 46920366)
51. Type 1 inositol trisphosphate receptor regulates cerebellar circuits by maintaining the spine morphology of purkinje cells in adult mice. Sugawara T, Hisatsune C, Le TD, Hashikawa T, Hirono M, Hattori M, Nagao S, Mikoshiba K, J Neurosci 2013 33 12186 12196 10.1523/JNEUROSCI.0545-13.2013 23884927
52. Double dissociation between long-term depression and dendritic spine morphology in cerebellar Purkinje cells. Sdrulla AD, Linden DJ, Nat Neurosci 2007 10 546 548 10.1038/nn1889 17435753 (Pubitemid 46652445)
53. Assessing the efficacy of specific cerebellomodulatory drugs for use as therapy for spinocerebellar ataxia type 1. Nag N, Tarlac V, Storey E, Cerebellum 2013 12 74 82 10.1007/s12311-012-0399-x 22718440
54. Aminopyridines correct early dysfunction and delay neurodegeneration in a mouse model of spinocerebellar ataxia type 1. Hourez R, Servais L, Orduz D, Gall D, Millard I, de Kerchove d'Exaerde A, Cheron G, Orr HT, Pandolfo M, Schiffmann SN, J Neurosci 2011 31 11795 11807 10.1523/JNEUROSCI.0905-11.2011 21849540
55. 3,4-diaminopyridine for the treatment of Lambert-Eaton myasthenic syndrome. Wirtz PW, Titulaer MJ, Gerven JM, Verschuuren JJ, Expert Rev Clin Immunol 2010 6 867 874 10.1586/eci.10.57 20979551
56. Lithium therapy improves neurological function and hippocampal dendritic arborization in a spinocerebellar ataxia type 1 mouse model. Watase K, Gatchel JR, Sun Y, Emamian E, Atkinson R, Richman R, Mizusawa H, Orr HT, Shaw C, Zoghbi HY, PLoS Med 2007 4 182 10.1371/journal.pmed.0040182 17535104 (Pubitemid 46842575)
57. Cerebellar lithium toxicity: a review of recent literature and tentative pathophysiology. Grignon S, Bruguerolle B, Therapie 1996 51 101 106 8763043
58. Exciting times beyond the brain: metabotropic glutamate receptors in peripheral and non-neural tissues. Julio-Pieper M, Flor PJ, Dinan TG, Cryan JF, Pharmacol Rev 2011 63 35 58 10.1124/pr.110.004036 21228260
59. Melanoma mouse model implicates metabotropic glutamate signaling in melanocytic neoplasia. Pollock PM, Cohen-Solal K, Sood R, Namkoong J, Martino JJ, Koganti A, Zhu H, Robbins C, Makalowska I, Shin SS, Marin Y, Roberts KG, Yudt LM, Chen A, Cheng J, Incao A, Pinkett HW, Graham CL, Dunn K, Crespo-Carbone SM, Mackason KR, Ryan KB, Sinsimer D, Goydos J, Reuhl KR, Eckhaus M, Meltzer PS, Pavan WJ, Trent JM, Chen S, Nat Genet 2003 34 108 112 10.1038/ng1148 12704387 (Pubitemid 36548800)
60. Functional effects of GRM1 suppression in human melanoma cells. Wangari-Talbot J, Wall BA, Goydos JS, Chen S, Mol Cancer Res 2012 10 1440 1450 10.1158/1541-7786.MCR-12-0158 22798429
61. Analysis of thick brain sections by obverse-reverse computer microscopy: application of a new, high clarity Golgi-Nissl stain. Glaser EM, Van der Loos H, J Neurosci Methods 1981 4 117 125 10.1016/0165-0270(81)90045-5 6168870 (Pubitemid 11005370)
62. A method for vibratome sectioning of Golgi-Cox stained whole rat brain. Gibb R, Kolb B, J Neurosci Methods 1998 79 1 4 10.1016/S0165-0270(97)00163-5 9531453 (Pubitemid 28248234)
63. The quantiative measurement of motor inco-ordination in naive mice using an acelerating rotarod. Jones BJ, Roberts DJ, J Pharm Pharmacol 1968 20 302 304 10.1111/j.2042-7158.1968.tb09743.x 4384609