Abnormal sensitivity of cannabinoid CB1 receptors in the striatum of mice with experimental amyotrophic lateral sclerosis

Amyotrophic Lateral Sclerosis

Volumn 11, Issue 1-2, 2010, Pages 83-90

  Rossi, Silvia ^a,b   De Chiara, Valentina ^a,b   Musella, Alessandra ^a,b   Cozzolino, Mauro ^b   Bernardi, Giorgio ^a,b   MacCarrone, Mauro ^b,c   Mercuri, Nicola B ^a,b   Carr, Maria Teresa ^d   Centonze, Diego ^a,b  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^c UNIVERSITY OF TERAMO   (Italy)

^d UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

ALS; CB1 receptors; Endocannabinoids; EPSC; IPSC

Indexed keywords

CANNABINOID 1 RECEPTOR; ENDOCANNABINOID; GLUTAMATE RECEPTOR; GLUTAMIC ACID;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN NERVE CELL; BRAIN SLICE; CONTROLLED STUDY; CORPUS STRIATUM; EXCITATORY POSTSYNAPTIC POTENTIAL; GABAERGIC TRANSMISSION; MOUSE; NERVE CELL DEGENERATION; NEUROPHYSIOLOGY; NEUROTRANSMITTER RELEASE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; SYNAPSE; SYNAPTIC TRANSMISSION;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; EXCITATORY POSTSYNAPTIC POTENTIALS; GAMMA-AMINOBUTYRIC ACID; GENOTYPE; GLUTAMIC ACID; MALE; MICE; MICE, MUTANT STRAINS; NERVE DEGENERATION; NEURAL INHIBITION; NEUROPROTECTIVE AGENTS; RECEPTOR, CANNABINOID, CB1; SUPEROXIDE DISMUTASE; SYNAPTIC TRANSMISSION; TETRAHYDROCANNABINOL;

EID: 77649303871     PISSN: 17482968     EISSN: 1471180X     Source Type: Journal    
DOI: 10.3109/17482960902977954     Document Type: Article

References (53)

1. Bruijn LI, Miller TM, Cleveland DW. Unravelling the mechanisms involved in motor neuron degeneration in ALS. Annu Rev Neurosci. 2004;27:723-49.
2. Nirmalananthan N, Greensmith L. Amyotrophic lateral sclerosis: recent advances and future therapies. Curr Opin Neurol. 2005;18:712-9.
3. Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, Hentati A, et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature. 1993;362:59-62.
4. Shaw CE, Enayat ZE, Chioza BA, Al-Chalabi A, Radunovic A, Powell JF, et al. Mutations in all five exons of SOD1 may cause ALS. Ann Neurol. 1998;43:390-4.
5. Takahashi H, Snow BJ, Bhatt MH, Peppard R, Eisen A, Calne DB. Evidence for a dopaminergic deficit in sporadic amyotrophic lateral sclerosis on positron emission scanning. Lancet. 1993;342:1016-8.
6. Desai J, Swash M. Extrapyramidal involvement in amyotrophic lateral sclerosis: backward falls and retropulsion. J Neurol Neurosurg Psychiatry. 1999;67:214-6.
7. Petrik MS, Wilson JM, Grant SC, Blackband SJ, Tabata RC, Shan X, et al. Magnetic resonance microscopy and immunohistochemistry of the CNS of the mutant SOD murine model of ALS reveals widespread neural deficits. Neuromolecular Med. 2007;9:216-29.
8. Gurney ME, Pu H, Chiu AY, Dal Canto MC, Polchow CY, Alexander DD, et al. Motor neuron degeneration in mice that express a human Cu/Zn superoxide dismutase mutation. Science. 1994;264:1772-5. (Pubitemid 24227760)
9. Pardo CA, Xu Z, Borchelt DR, Price DL, Sisodia SS, Cleveland DW. Superoxide dismutase is an abundant component in cell bodies, dendrites, and axons of motor neurons and in a subset of other neurons. Proc Natl Acad Sci USA. 1995;92:954-8.
10. Siemiatkowski M, Rokicki D, Czl onkowska AI, Sienkiewicz-Jarosz H, Bidziń ski A, Pl aźnik A. Locomotor activity and a conditioned fear response: correlation with cortical and subcortical binding of the dopamine D1 receptor antagonist. Neuroreport. 2000;11:3953-6.
11. Geracitano R, Paolucci E, Prisco S, Guatteo E, Zona C, Longone P, et al. Altered long-term corticostriatal synaptic plasticity in transgenic mice overexpressing human Cu/Zn superoxide dismutase (GLY(93)-(ALA) mutation. Neuroscience. 2003;118:399-408.
12. Centonze D, Battista N, Rossi S, Mercuri NB, Finazzi-Agro A, Bernardi G, et al. A critical interaction between dopamine D2 receptors and endocannabinoids mediates the effects of cocaine on striatal GABAergic transmission. Neuropsychopharmacology. 2004;29:1488-97.
13. Pan B, Hillard CJ, Liu QS. D2 dopamine receptor activation facilitates endocannabinoid-mediated long-term synaptic depression of GABAergic synaptic transmission in midbrain dopamine neurons via cAMP-protein kinase A signalling. J Neurosci. 2008;28:14018-30.
14. Piomelli D. The molecular logic of endocannabinoid signalling. Nat Rev Neurosci. 2003;4:873-84.
15. Raman C, McAllister SD, Rizvi G, Patel SG, Moore DH, Abood ME. Amyotrophic lateral sclerosis: delayed disease progression in mice by treatment with a cannabinoid. Amyotroph Lateral Scler Other Motor Neuron Disord. 2004;5:33-9.
16. Witting A, Weydt P, Hong S, Kliot M, Moller T, Stella N. Endocannabinoids accumulate in spinal cord of SOD1-G93A transgenic mice. J Neurochem. 2004;89:1555-7.
17. Weydt P, Hong S, Witting A, Möller T, Stella N, Kliot M. Cannabinol delays symptom onset in SOD1-G93A transgenic mice without affecting survival. Amyotroph Lateral Scler Other Motor Neuron Disord. 2005;6:182-4.
18. Bilsland LG, Dick JR, Pryce G, Petrosino S, Di Marzo V, Baker D, et al. Increasing cannabinoid levels by pharmacological and genetic manipulation delay disease progression in SOD1 mice. FASEB J. 2006;20:1003-5.
19. Shoemaker JL, Seely KA, Reed RL, Crow JP, Prather PL. The CB2 cannabinoid agonist AM-1241 prolongs survival in a transgenic mouse model of amyotrophic lateral sclerosis when initiated at symptom onset. J Neurochem. 2007; 101:87-98.
20. Zhao P, Ignacio S, Beattie EC, Abood ME. Altered presymptomatic AMPA and cannabinoid receptor trafficking in motor neurons of ALS model mice: implications for excitotoxicity. Eur J Neurosci. 2008;27:572-9.
21. Rothstein JD, van Kammen M, Levey AI, Martin LJ, Kuncl RW. Selective loss of glial glutamate transporter GLT-1 in amyotrophic lateral sclerosis. Ann Neurol. 1995;38:73-84.
22. Roy J, Minotti S, Dong L, Figlewicz DA, Durham HD. Glutamate potentiates the toxicity of mutant Cu/Zn superoxide dismutase in motor neurons by postsynaptic calciumdependent mechanisms. J Neurosci. 1998;18:9673-84.
23. van den Bosch L, van den BergheW, Klaassen H, van Houtte E, Robberecht W. Ca(2-)-permeable AMPA receptors and selective vulnerability of motor neurons. J Neurol Sci. 2000;180:29-34.
24. Pieri M, Gaetti C, Spalloni A, Cavalcanti S, Mercuri N, Bernardi G, et al. Alpha-amino-3-hydroxy-5-methyl-isoxazole-4-propionate receptors in spinal cord motor neurons are altered in transgenic mice overexpressing human Cu/Zn superoxide dismutase (Gly93--Ala) mutation. Neuroscience. 2003;122:47-58.
25. Kawahara Y, Kwak S. Excitotoxicity and ALS: what is unique about the AMPA receptors expressed on spinal motor neurons? Amyotroph Lateral Scler Other Motor Neuron Disord. 2005;6:131-44.
26. Tortarolo M, Grignaschi G, Calvaresi N, Zennaro E, Spaltro G, Colovic M, et al. Glutamate AMPA receptors change in motor neurons of SOD1-G93A transgenic mice and their inhibition by a non-competitive antagonist ameliorates the progression of amyotrophic lateral sclerosis-like disease. J Neurosci Res. 2006;83:134-46.
27. Centonze D, Rossi S, Prosperetti C, Tscherter A, Bernardi G, Maccarrone M, et al. Abnormal sensitivity to cannabinoid receptor stimulation might contribute to altered gammaaminobutyric acid transmission in the striatum of R6/2 Huntington's disease mice. Biol Psychiatry. 2005;57:1583-9.
28. Centonze D, Bari M, Rossi S, Prosperetti C, Furlan R, Fezza F, et al. The endocannabinoid system is dysregulated in multiple sclerosis and in experimental autoimmune encephalomyelitis. Brain. 2007;130:2543-53.
29. Centonze D, Rossi S, de Chiara V, Prosperetti C, Battista N, Bernardi G, et al. Chronic cocaine sensitizes striatal GABAergic synapses to the stimulation of cannabinoid CB1 receptors. Eur J Neurosci. 2007;25:1631-40.
30. Rossi S, de Chiara V, Musella A, Kusayanagi H, Mataluni G, Bernardi G, et al. Chronic psychoemotional stress impairs cannabinoid-receptor-mediated control of GABA transmission in the striatum. J Neurosci. 2008;28:7284-92.
31. Szabo B, Urbanski MJ, Bisogno T, Di Marzo V, Mendiguren A, Baer WU, et al. Depolarization-induced retrograde synaptic inhibition in the mouse cerebellar cortex is mediated by 2-arachidonoylglycerol. J Physiol. 2006;577:263-80.
32. Gerdeman G, Lovinger DM. CB1 cannabinoid receptor inhibits synaptic release of glutamate in rat dorsolateral striatum. J Neurophysiol. 2001;85:468-71.
33. Andersson M, Usiello A, Borgkvist A, Pozzi L, Dominguez C, Fienberg AA, et al. Cannabinoid action depends on phosphorylation of dopamine-and cAMP-regulated phosphoprotein of 32 kDa at the protein kinase A site in striatal projection neurons. J Neurosci. 2005;25:8432-8.
34. Ade KK, Lovinger DM. Anandamide regulates postnatal development of long-term synaptic plasticity in the rat dorsolateral striatum. J Neurosci. 2007;27:2403-9.
35. Cozzolino M, Amori I, Pesaresi MG, Ferri A, Nencini M, Carr̀ MT. Cysteine 111 affects aggregation and cytotoxicity of mutant Cu/Zn superoxide dismutase associated with familial amyotrophic lateral sclerosis. J Biol Chem. 2008;283:866-74.
36. Zhang B, Tu P, Abtahian F, Trojanowski JQ, Lee VM. Neurofilaments and orthograde transport are reduced in ventral root axons of transgenic mice that express human SOD1 with a G93A mutation. J Cell Biol. 1997;139: 1307-15.
37. Williamson TL, Cleveland DW. Slowing of axonal transport is a very early event in the toxicity of ALS-linked SOD1 mutants to motor neurons. Nat Neurosci. 1999;2:50-6.
38. Gubellini P, Picconi B, Bari M, Battista N, Calabresi P, Centonze D, et al. Experimental Parkinsonism alters endocannabinoid degradation: implications for striatal glutamatergic transmission. J Neurosci. 2002;22:6900-7.
39. Hansen HH, Azcoitia I, Pons S, Romero J, Garc?́a-Segura LM, Ramos JA, et al. Blockade of cannabinoid CB(1) receptor function protects against in vivo disseminating brain damage following NMDA-induced excitotoxicity. J Neurochem. 2002;82:154-8.
40. Hansen HH, Krutz B, Sifringer M, Stefovska V, Bittigau P, Pragst F, et al. Cannabinoids enhance susceptibility of immature brain to ethanol neurotoxicity. Ann Neurol. 2008;64:42-52.
41. Downer EJ, Fogarty MP, Campbell VA. Tetrahydrocannabinol-induced neurotoxicity depends on CB1 receptormediated c-Jun N-terminal kinase activation in cultured cortical neurons. Br J Pharmacol. 2003;140:547-57.
42. Downer EJ, Gowran A, Murphy AC, Campbell VA. The tumour suppressor protein, p53, is involved in the activation of the apoptotic cascade by Delta9-tetrahydrocannabinol in cultured cortical neurons. Eur J Pharmacol. 2007;564:57-65.
43. Shen M, Thayer SA. Cannabinoid receptor agonists protect cultured rat hippocampal neurons from excitotoxicity. Mol Pharmacol. 1998;54:459-62.
44. Marsicano G, Goodenough S, Monory K, Hermann H, Eder M, Cannich A, et al. CB1 cannabinoid receptors and ondemand defence against excitotoxicity. Science. 2003;302: 84-8.
45. Pryce G, Ahmed Z, Hankey DJ, Jackson SJ, Croxford JL, Pocock JM, et al. Cannabinoids inhibit neurodegeneration in models of multiple sclerosis. Brain. 2003;126:2191-202.
46. Gilbert GL, Kim HJ, Waataja JJ, Thayer SA. Delta9-tetrahydrocannabinol protects hippocampal neurons from excitotoxicity. Brain Res. 2007;1128:61-9.
47. Nagayama T, Sinor AD, Simon RP, Chen J, Graham SH, Jin K, et al. Cannabinoids and neuroprotection in global and focal cerebral ischaemia and in neuronal cultures. J Neurosci. 1999;19:2987-95.
48. van der Stelt M, Veldhuis WB, van Haaften GW, Fezza F, Bisogno T, Bar PR, et al. Exogenous anandamide protects rat brain against acute neuronal injury in vivo. J Neurosci. 2001;21:8765-71.
49. Facchinetti F, del Giudice E, Furegato S, Passarotto M, Leon A. Cannabinoids ablate release of TNFalpha in rat microglial cells stimulated with lypopolysaccharide. Glia. 2003;41: 161-8.
50. Puffenbarger RA, Boothe AC, Cabral GA. Cannabinoids inhibit LPS-inducible cytokine mRNA expression in rat microglial cells. Glia. 2000;29:58-69.
51. McGeer PL, McGeer EG. Inflammatory processes in amyotrophic lateral sclerosis. Muscle Nerve. 2002;26:459-70.
52. Liang X, Wang Q, Shi J, Lokteva L, Breyer RM, Montine TJ, et al. The prostaglandin E2 EP2 receptor accelerates disease progression and inflammation in a model of amyotrophic lateral sclerosis. Ann Neurol. 2008;64:304-14.
53. Boillée S, van de Velde C, Cleveland DW. ALS: a disease of motor neurons and their non-neuronal neighbours. Neuron. 2006;52:39-59.