Knocking down metabotropic glutamate receptor 1 improves survival and disease progression in the SOD1G93A mouse model of amyotrophic lateral sclerosis

Neurobiology of Disease

Volumn 64, Issue , 2014, Pages 48-59

  Milanese, Marco ^a   Giribaldi, Francesco ^a   Melone, Marcello ^b,d   Bonifacino, Tiziana ^a   Musante, Ilaria ^a,c   Carminati, Enrico ^a   Rossi, Pia I A ^a,c   Vergani, Laura ^a   Voci, Adriana ^a   Conti, Fiorenzo ^b,d   Puliti, Aldamaria ^a,c   Bonanno, Giambattista ^a  

^a UNIVERSITY OF GENOA   (Italy)

^b UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^c INRCA   (Italy)

^d G GASLINI INSTITUTE   (Italy)

Author keywords

Amyotrophic lateral sclerosis; Disease development; Glutamate transmission; Metabotropic glutamate type 1 receptor; Metabotropic glutamate type 1 receptor knocking down; Metabotropic glutamate type 5 receptor; SOD1G93A mouse

Indexed keywords

CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; GLUTAMIC ACID; MESSENGER RNA; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR 5; METALLOTHIONEIN;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; CELL DAMAGE; CONTROLLED STUDY; DISEASE COURSE; EXCITOTOXICITY; EXPERIMENTAL MODEL; FEMALE; GENE SILENCING; GLIOSIS; MALE; MITOCHONDRION; MOLECULAR PATHOLOGY; MOTONEURON; MOTOR PERFORMANCE; MOUSE; MOUSE MUTANT; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPONTANEOUS MUTATION; SURVIVAL;

AMYOTROPHIC LATERAL SCLEROSIS; DISEASE DEVELOPMENT; GLUTAMATE TRANSMISSION; METABOTROPIC GLUTAMATE TYPE 1 RECEPTOR; METABOTROPIC GLUTAMATE TYPE 1 RECEPTOR KNOCKING DOWN; METABOTROPIC GLUTAMATE TYPE 5 RECEPTOR; SOD1(G93A) MOUSE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ASTROCYTES; CATALASE; DISEASE PROGRESSION; EXCITATORY AMINO ACID TRANSPORTER 2; GLUTAMIC ACID; METALLOTHIONEIN; MICE; MICE, TRANSGENIC; MICROGLIA; MITOCHONDRIA; MOTOR ACTIVITY; MOTOR NEURONS; POINT MUTATION; RECEPTOR, METABOTROPIC GLUTAMATE 5; RECEPTORS, METABOTROPIC GLUTAMATE; RNA, MESSENGER; SEVERITY OF ILLNESS INDEX; SPINAL CORD; SUPEROXIDE DISMUTASE; SURVIVAL ANALYSIS;

EID: 84892455543     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2013.11.006     Document Type: Article

References (71)

1. Andersen P.M., Al-Chalabi A. Clinical genetics of amyotrophic lateral sclerosis: what do we really know?. Nat. Rev. Neurol. 2011, 7:603-615.
2. Babu G.N., Kumar A., Chandra R., Puri S.K., Singh R.L., Kalita J., et al. Oxidant-antioxidant imbalance in the erythrocytes of sporadic amyotrophic lateral sclerosis patients correlates with the progression of disease. Neurochem. Int. 2008, 52:1284-1289.
3. Beers D.R., Henkel J.S., Xiao Q., Zhao W., Wang J., Yen A.A., et al. Wild-type microglia extend survival in PU.1 knockout mice with familial amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:16021-16026.
4. Berg D., Godau J., Trenkwalder C., Eggert K., Csoti I., Storch A., et al. AFQ056 treatment of levodopa-induced dyskinesias: results of 2 randomized controlled trials. Mov. Disord. 2011, 26:1243-1250.
5. Berry-Kravis E., Hessl D., Coffey S., Hervey C., Schneider A., Yuhas J., et al. A pilot open label, single dose trial of fenobam in adults with fragile X syndrome. J. Med. Genet. 2009, 46:266-271.
6. Bilsland L.G., Sahai E., Kelly G., Golding M., Greensmith L., Schiavo G. Deficits in axonal transport precede ALS symptoms in vivo. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:20523-20528.
7. Birve A., Neuwirth C., Weber M., Marklund S.L., Nilsson A.C., Jonsson P.A., et al. A novel SOD1 splice site mutation associated with familial ALS revealed by SOD activity analysis. Hum. Mol. Genet. 2010, 19:4201-4206.
8. Boillée S., Vande Velde C., Cleveland D.W. ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron 2006, 52:39-59.
9. Boillée S., Yamanaka K., Lobsiger C.S., Copeland N.G., Jenkins N.A., Kassiotis G., et al. Onset and progression in inherited ALS determined by motor neurons and microglia. Science 2006, 312:1389-1392.
10. Boston-Howes W., Gibb S.L., Williams E.O., Pasinelli P., Brown R.H., Trotti D. Caspase-3 cleaves and inactivates the glutamate transporter EAAT2. J. Biol. Chem. 2006, 281:14076-14084.
11. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal. Biochem. 1976, 72:248-254.
12. Cheah B.C., Vucic S., Krishnan A.V., Kiernan M.C. Riluzole, neuroprotection and amyotrophic lateral sclerosis. Curr. Med. Chem. 2010, 17:1942-1959.
13. Cleveland D.W., Bruijn L.I., Wong P.C., Marszalek J.R., Vechio J.D., Lee M.K., et al. Mechanisms of selective motor neuron death in transgenic mouse models of motor neuron disease. Neurology 1996, 47(Suppl. 2):S54-S61. (discussion S61-S62).
14. Conn P.J., Pin J.P. Pharmacology and functions of metabotropic glutamate receptors. Annu. Rev. Pharmacol. Toxicol. 1997, 37:205-237.
15. Conti F., Weinberg R.J. Shaping excitation at glutamatergic synapses. Trends Neurosci. 1999, 22:451-458.
16. Conti V., Aghaie A., Cilli M., Martin N., Caridi G., Musante L., et al. 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. 2006, 18:593-600.
17. Cozzolino M., Carrì M.T. Mitochondrial dysfunction in ALS. Prog. Neurobiol. 2012, 97:54-66.
18. Cudkowicz M., Shefner J., Consortium N.E.A.L.S. STAGE 3 clinical trial of ceftriaxone in subjects with ALS (S36.001). Neurology 2013, 80:S36.001.
19. 2+ capacity impairment precedes the onset of motor symptoms in G93A Cu/Zn-superoxide dismutase mutant mice. J. Neurochem. 2006, 96:1349-1361.
20. De Blasi A., Conn P.J., Pin J., Nicoletti F. Molecular determinants of metabotropic glutamate receptor signaling. Trends Pharmacol. Sci. 2001, 22:114-120.
21. Dingledine R., Borges K., Bowie D., Traynelis S.F. The glutamate receptor ion channels. Pharmacol. Rev. 1999, 51:7-61.
22. Doble A. The role of excitotoxicity in neurodegenerative disease: implications for therapy. Pharmacol. Ther. 1999, 81:163-221.
23. Dunlop J., Beal McIlvain H., She Y., Howland D.S. Impaired spinal cord glutamate transport capacity and reduced sensitivity to riluzole in a transgenic superoxide dismutase mutant rat model of amyotrophic lateral sclerosis. J. Neurosci. 2003, 23:1688-1696.
24. Fazio F., Notartomaso S., Aronica E., Storto M., Battaglia G., Vieira E., et al. 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. Neuropharmacology 2008, 55:491-499.
25. Ferraguti F., Crepaldi L., Nicoletti F. Metabotropic glutamate 1 receptor: current concepts and perspectives. Pharmacol. Rev. 2008, 60:536-581.
26. Ferraiuolo L., Kirby J., Grierson A.J., Sendtner M., Shaw P.J. Molecular pathways of motor neuron injury in amyotrophic lateral sclerosis. Nat. Rev. Neurol. 2011, 7:616-630.
27. Fleck M.W., Barrionuevo G., Palmer A.M. Synaptosomal and vesicular accumulation of l-glutamate, l- aspartate and d-aspartate. Neurochem. Int. 2001, 39:217-225.
28. +-dependent glutamate transporter GLT1 by a neuroimmunophilin ligand results in neuroprotection. Neurobiol. Dis. 2006, 21:556-567.
29. Giribaldi F., Milanese M., Bonifacino T., Rossi P.I.A., Di Prisco S., Pittaluga A., et al. Group I metabotropic glutamate autoreceptors induce abnormal glutamate exocytosis in a mouse model of amyotrophic lateral sclerosis. Neuropharmacology 2013, 66:253-263.
30. Gong Y.H., Elliott J.L. Metallothionein expression is altered in a transgenic murine model of familial amyotrophic lateral sclerosis. Exp. Neurol. 2000, 162:27-36.
31. Gurney M.E., Pu H., Chiu A.Y., Dal Canto M.C., Polchow C.Y., Alexander D.D., et al. Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science 1994, 264:1772-1775. (Erratum in: Science 269, 149).
32. Heath P.R., Shaw P.J. Update on the glutamatergic neurotransmitter system and the role of excitotoxicity in amyotrophic lateral sclerosis. Muscle Nerve 2002, 26:438-458.
33. Howland D.S., Liu J., She Y., Goad B., Maragakis N.J., Kim B., et al. Focal loss of the glutamate transporter EAAT2 in a transgenic rat model of SOD1 mutant-mediated amyotrophic lateral sclerosis (ALS). Proc. Natl. Acad. Sci. U. S. A. 2002, 99:1604-1609.
34. Ilieva H., Polymenidou M., Cleveland D.W. Non-cell autonomous toxicity in neurodegenerative disorders: ALS and beyond. J. Cell Biol. 2009, 187:761-772.
35. Jaarsma D., Haasdijk E.D., Grashorn J.A., Hawkins R., van Duijn W., Verspaget H.W., et al. Human Cu/Zn superoxide dismutase (SOD1) overexpression in mice causes mitochondrial vacuolization, axonal degeneration, and premature motoneuron death and accelerates motoneuron disease in mice expressing a familial amyotrophic lateral sclerosis mutant SOD1. Neurobiol. Dis. 2000, 7(6 Pt B):623-643.
36. Jaarsma D., Rognoni F., van Duijn W., Verspaget H.W., Haasdijk E.D., Holstege J.C. CuZn superoxide dismutase (SOD1) accumulates in vacuolated mitochondria in transgenic mice expressing amyotrophic lateral sclerosis-linked SOD1 mutations. Acta Neuropathol. 2001, 102:293-305.
37. Lanza C., Morando S., Voci A., Canesi L., Principato M.C., Serpero L.D., et al. Neuroprotective mesenchymal stem cells are endowed with a potent antioxidant effect in vivo. J. Neurochem. 2009, 110:1674-1684.
38. Lasiene J., Yamanaka K. Glial cells in amyotrophic lateral sclerosis. Neurol. Res. Int. 2011, 718987.
39. Levenga J., Hayashi S., de Vrij F.M., Koekkoek S.K., van der Linde H.C., Nieuwenhuizen I., et al. AFQ056, a new mGluR5 antagonist for treatment of fragile X syndrome. Neurobiol. Dis. 2011, 42:311-317.
40. Li Q., Spencer N.Y., Pantazis N.J., Engelhardt J.F. Alsin and SOD1(G93A) proteins regulate endosomal reactive oxygen species production by glial cells and proinflammatory pathways responsible for neurotoxicity. J. Biol. Chem. 2011, 286:40151-40162.
41. Lin M.T., Beal M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006, 443:787-795.
42. Milanese M., Zappettini S., Jacchetti E., Bonifacino T., Cervetto C., Usai C., et al. 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. 2010, 113:489-501.
43. Milanese M., Zappettini S., Onofri F., Musazzi L., Tardito D., Bonifacino T., et al. Abnormal exocytotic release of glutamate in a mouse model of amyotrophic lateral sclerosis. J. Neurochem. 2011, 116:1028-1042.
44. Nicoletti F., Bockaert J., Collingridge G.L., Conn P.J., Ferraguti F., Schoepp D.D., et al. Metabotropic glutamate receptors: from the workbench to the bedside. Neuropharmacology 2011, 60:1017-1041.
45. Nikolić-Kokić A., Stević Z., Blagojević D., Davidović B., Jones D.R., Spasić M.B. Alterations in anti-oxidative defence enzymes in erythrocytes from sporadic amyotrophic lateral sclerosis (SALS) and familial ALS patients. Clin. Chem. Lab. Med. 2006, 44:589-593.
46. Ono S., Endo Y., Tokuda E., Ishige K., Tabata K., Asami S., et al. Upregulation of metallothionein-I mRNA expression in a rodent model for amyotrophic lateral sclerosis. Biol. Trace Elem. Res. 2006, 113:93-104.
47. Parone P.A., Da Cruz S., Han J.S., McAlonis-Downes M., Vetto A.P., Lee S.K., et al. Enhancing mitochondrial calcium buffering capacity reduces aggregation of misfolded SOD1 and motor neuron cell death without extending survival in mouse models of inherited amyotrophic lateral sclerosis. J. Neurosci. 2013, 33:4657-4671.
48. Perry T.L., Krieger C., Hansen S., Eisen A. Amyotrophic lateral sclerosis: amino acid levels in plasma and cerebrospinal fluid. Ann. Neurol. 1990, 28:12-17.
49. Porter R.H., Jaeschke G., Spooren W., Ballard T.M., Büttelmann B., Kolczewski S., et al. Fenobam: a clinically validated nonbenzodiazepine anxiolytic is a potent, selective, and noncompetitive mGlu5 receptor antagonist with inverse agonist activity. J. Pharmacol. Exp. Ther. 2005, 315:711-721.
50. Raiteri M., Bonanno G., Marchi M., Maura G. Is there a functional linkage between neurotransmitter uptake mechanisms and presynaptic receptors?. J. Pharmacol. Exp. Ther. 1984, 231:671-677.
51. Raiteri L., Paolucci E., Prisco S., Raiteri M., Bonanno G. Activation of a glycine transporter on spinal cord neurons causes enhanced glutamate release in a mouse model of amyotrophic lateral sclerosis. Br. J. Pharmacol. 2003, 138:1021-1025.
52. Raiteri L., Stigliani S., Zappettini S., Mercuri N.B., Raiteri M., Bonanno G. Excessive and precocious glutamate release in a mouse model of amyotrophic lateral sclerosis. Neuropharmacology 2004, 46:782-792.
53. Robberecht W. Oxidative stress in amyotrophic lateral sclerosis. J. Neurol. 2000, 247(Suppl. 1):I1-I6.
54. Rosen D.R., Siddique T., Patterson D., Figlewicz D.A., Sapp P., Hentati A., et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993, 364:59-62.
55. Rossi D., Brambilla L., Valori C.F., Roncoroni C., Crugnola A., Yokota T., et al. Focal degeneration of astrocytes in amyotrophic lateral sclerosis. Cell Death Differ. 2008, 15:1691-1700.
56. Rossi P.I., Musante I., Summa M., Pittaluga A., Emionite L., Ikehata M., et al. Compensatory molecular and functional mechanisms in nervous system of the Grm1crv4 mouse lacking the mGlu1 receptor: a model for motor coordination deficits. Cereb. Cortex 2012, 23(9):2179-2189.
57. Rothstein J.D. Excitotoxicity and neurodegeneration in amyotrophic lateral sclerosis. Clin. Neurosci. 1995, 3:348-359.
58. Rothstein J.D., Martin L.J., Kuncl R.W. Decreased glutamate transport by the brain and spinal cord in amyotrophic lateral sclerosis. N. Engl. J. Med. 1992, 326:1464-1468.
59. Rothstein J.D., Van Kammen M., Levey A.I., Martin L.J., Kuncl R.W. Selective loss of glial glutamate transporter GLT-1 in amyotrophic lateral sclerosis. Ann. Neurol. 1995, 38:73-84.
60. Rothstein J.D., Patel S., Regan M.R., Haenggeli C., Huang Y.H., Bergles D.E., et al. Beta-lactam antibiotics offer neuroprotection by increasing glutamate transporter expression. Nature 2005, 433:73-77.
61. Sasaki S., Warita H., Murakami T., Abe K., Iwata M. Ultrastructural study of mitochondria in the spinal cord of transgenic mice with a G93A mutant SOD1 gene. Acta Neuropathol. 2004, 107:461-474.
62. Shaw P.J., Eggett C.J. Molecular factors underlying selective vulnerability of motor neurons to neurodegeneration in amyotrophic lateral sclerosis. J. Neurol. 2000, 247(Suppl. 1):I17-I27.
63. 2+ homeostasis. J. Biol. Chem. 2010, 285:631-643.
64. Tortarolo M., Grignaschi G., Calvaresi N., Zennaro E., Spaltro G., Colovic M., et al. Glutamate AMPA receptors change in motor neurons of SOD1G93A transgenic mice and their inhibition by a noncompetitive antagonist ameliorates the progression of amyotrophic lateral sclerosis-like disease. J. Neurosci. Res. 2006, 83:134-146.
65. Trotti D., Aoki M., Pasinelli P., Berger U.V., Danbolt N.C., Brown R.H., et al. Amyotrophic lateral sclerosis-linked glutamate transporter mutant has impaired glutamate clearance capacity. J. Biol. Chem. 2001, 276:576-582.
66. Uccelli A., Milanese M., Principato M.C., Morando S., Bonifacino T., Vergani L., et al. Intravenous mesenchymal stem cells improve survival and motor function in experimental amyotrophic lateral sclerosis. Mol. Med. 2012, 18:794-804.
67. Van Damme P., Bogaert E., Dewil M., Hersmus N., Kiraly D., Scheveneels W., et al. Astrocytes regulate GluR2 expression in motor neurons and their vulnerability to excitotoxicity. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:14825-14830.
68. Wang L., Gutmann D.H., Roos R.P. Astrocyte loss of mutant SOD1 delays ALS disease onset and progression in G85R transgenic mice. Hum. Mol. Genet. 2011, 20:286-293.
69. Wang L., Popko B., Roos R.P. The unfolded protein response in familial amyotrophic lateral sclerosis. Hum. Mol. Genet. 2011, 20:1008-1015.
70. Watson C., Paxinos G., Kayalioglu G. The Spinal Cord 2008, Academic Press, Amsterdam.
71. Yamanaka K., Chun S.J., Boillee S., Fujimori-Tonou N., Yamashita H., Gutmann D.H., et al. Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis. Nat. Neurosci. 2008, 11:251-253.