Endocannabinoids and amyotrophic lateral sclerosis

Cannabinoids in Neurologic and Mental Disease

Volumn , Issue , 2015, Pages 99-123

  de Lago, Eva ^a,b   Moreno Martet, Miguel ^a,b   Espejo Porras, Francisco ^a,b   Fernández Ruiz, Javier ^a,b  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

Author keywords

Amyotrophic lateral sclerosis; Cannabinoids; CB1 receptors; CB2 receptors; Endocannabinoid signaling system; Motor neuron injury; Neurodegeneration; Neuroprotection

Indexed keywords

EID: 84931011233     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-0-12-417041-4.00005-9     Document Type: Chapter

References (123)

1. Ackerley S., Grierson A.J., Brownlees J., Thornhill P., Anderton B.H., Leigh P.N., et al. Glutamate slows axonal transport of neurofilaments in transfected neurons. J. Cell Biol. 2000, 150:165-176.
2. Ackerley S., Grierson A.J., Banner S., Perkinton M.S., Brownlees J., Byers H.L., et al. p38alpha stress-activated protein kinase phosphorylates neurofilaments and is associated with neurofilament pathology in amyotrophic lateral sclerosis. Mol. Cell. Neurosci. 2004, 26:354-364.
3. Ahmed A., Wicklund M.P. Amyotrophic lateral sclerosis: what role does environment play?. Neurol. Clin. 2011, 29:689-711.
4. Al-Chalabi A., Hardiman O. The epidemiology of ALS: a conspiracy of genes, environment and time. Nat. Rev. Neurol. 2013, 9:617-628.
5. Amtmann D., Weydt P., Johnson K.L., Jensen M.P., Carter G.T. Survey of cannabis use in patients with amyotrophic lateral sclerosis. Am. J. Hosp. Palliat. Care 2004, 21:95-104.
6. Andersen P.M., Al-Chalabi A. Clinical genetics of amyotrophic lateral sclerosis: what do we really know?. Nat. Rev. Neurol. 2011, 7:603-615.
7. Ash P.E., Bieniek K.F., Gendron T.F., Caulfield T., Lin W.L., Dejesus-Hernandez M., et al. Unconventional translation of C9ORF72 GGGGCC expansion generates insoluble polypeptides specific to c9FTD/ALS. Neuron 2013, 77:639-646.
8. Atkin J.D., Farg M.A., Turner B.J., Tomas D., Lysaght J.A., Nunan J., et al. Induction of the unfolded protein response in familial amyotrophic lateral sclerosis and association of protein-disulfide isomerase with superoxide dismutase 1. J. Biol. Chem. 2006, 281:30152-30165.
9. Atkin J.D., Farg M.A., Walker A.K., McLean C., Tomas D., Horne M.K. Endoplasmic reticulum stress and induction of the unfolded protein response in human sporadic amyotrophic lateral sclerosis. Neurobiol. Dis. 2008, 30:400-407.
10. Barber S.C., Shaw P.J. Oxidative stress in ALS: key role in motor neuron injury and therapeutic target. Free Radic. Biol. Med. 2010, 48:629-641.
11. Benatar M. Lost in translation: treatment trials in the SOD1 mouse and in human ALS. Neurobiol. Dis. 2007, 26:1-13.
12. Berry J.D., Shefner J.M., Conwit R., Schoenfeld D., Keroack M., Felsenstein D., et al. Design and initial results of a multi-phase randomized trial of ceftriaxone in amyotrophic lateral sclerosis. PLOS ONE 2013, 8:e61177.
13. Bilsland L.G., Dick J.R., 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, 20:1003-1005.
14. Bordet T., Buisson B., Michaud M., Drouot C., Galéa P., Delaage P., et al. Identification and characterization of cholest-4-en-3-one, oxime (TRO19622), a novel drug candidate for amyotrophic lateral sclerosis. J. Pharmacol. Exp. Ther. 2007, 322:709-720.
15. Bosco D.A., Morfini G., Karabacak N.M., Song Y., Gros-Louis F., Pasinelli P., et al. Wild-type and mutant SOD1 share an aberrant conformation and a common pathogenic pathway in ALS. Nat. Neurosci. 2010, 13:1396-1403.
16. 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.
17. Bova M.P., Kinney G.G. Emerging drug targets in amyotrophic lateral sclerosis. Expert Opin. Orph. Drugs 2013, 1:5-20.
18. Buratti E., Baralle F.E. The multiple roles of TDP-43 in pre-mRNA processing and gene expression regulation. RNA Biol. 2010, 7:420-429.
19. Camu W., Tremblier B., Plassot C., Alphandery S., Salsac C., Pageot N., et al. Vitamin D confers protection to motoneurons and is a prognostic factor of amyotrophic lateral sclerosis. Neurobiol. Aging 2014, 35:1198-1205.
20. Carter G.T., Abood M.E., Aggarwal S.K., Weiss M.D. Cannabis and amyotrophic lateral sclerosis: hypothetical and practical applications, and a call for clinical trials. Am. J. Hosp. Palliat. Care 2010, 27:347-356.
21. Cashman N.R., Durham H.D., Blusztajn J.K., Oda K., Tabira T., Shaw I.T., et al. Neuroblastoma x spinal cord (NSC) hybrid cell lines resemble developing motor neurons. Dev. Dyn. 1992, 194:209-221.
22. Cheah B.C., Vucic S., Krishnan A.V., Kiernan M.C. Riluzole, neuroprotection and amyotrophic lateral sclerosis. Curr. Med. Chem. 2010, 17:194-199.
23. Chen H.J., Anagnostou G., Chai A., Withers J., Morris A., Adhikaree J., et al. Characterization of the properties of a novel mutation in VAPB in familial amyotrophic lateral sclerosis. J. Biol. Chem. 2010, 285:40266-40281.
24. Cox L.E., Ferraiuolo L., Goodall E.F., Heath P.R., Higginbottom A., Mortiboys H., et al. Mutations in CHMP2B in lower motor neuron predominant amyotrophic lateral sclerosis (ALS). PLOS ONE 2010, 5:e9872.
25. Cruts M., Gijselinck I., Van Langenhove T., van der Zee J., Van Broeckhoven C. Current insights into the C9orf72 repeat expansion diseases of the FTLD/ALS spectrum. Trends Neurosci. 2013, 36:450-459.
26. 2+ capacity impairment precedes the onset of motor symptoms in G93A Cu/Zn-superoxide dismutase mutant mice. J. Neurochem. 2006, 96:1349-1361.
27. DeJesús-Hernández M., Mackenzie I.R., Boeve B.F., Boxer A.L., Baker M., Rutherford N.J., et al. Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 2011, 72:245-256.
28. de Jong S., Huisman M., Sutedja N., van der Kooi A., de Visser M., Schelhaas J., et al. Endogenous female reproductive hormones and the risk of amyotrophic lateral sclerosis. J. Neurol. 2013, 260:507-512.
29. Deng H.X., Chen W., Hong S.T., Boycott K.M., Gorrie G.H., Siddique N., et al. Mutations in UBQLN2 cause dominant X-linked juvenile and adult-onset ALS and ALS/dementia. Nature 2011, 477:211-215.
30. De Vos K.J., Chapman A.L., Tennant M.E., Manser C., Tudor E.L., Lau K.F., et al. Familial amyotrophic lateral sclerosis-linked SOD1 mutants perturb fast axonal transport to reduce axonal mitochondria content. Hum. Mol. Genet. 2007, 16:2720-2728.
31. Dewil M., de la Cruz V.F., Van Den Bosch L., Robberecht W. Inhibition of p38 mitogen activated protein kinase activation and mutant SOD1(G93A)-induced motor neuron death. Neurobiol. Dis. 2007, 26:332-341.
32. Di Giorgio F.P., Boulting G.L., Bobrowicz S., Eggan K.C. Human embryonic stem cell-derived motor neurons are sensitive to the toxic effect of glial cells carrying an ALS-causing mutation. Cell Stem Cell 2008, 3:637-648.
33. Dormann D., Rodde R., Edbauer D., Bentmann E., Fischer I., Hruscha A., et al. ALS-associated fused in sarcoma (FUS) mutations disrupt transportin-mediated nuclear import. EMBO J. 2010, 29:2841-2857.
34. Fernández-Ruiz J., Romero J., Velasco G., Tolón R.M., Ramos J.A., Guzmán M. Cannabinoid CB2 receptor: a new target for controlling neural cell survival?. Trends Pharmacol. Sci. 2007, 28:39-45.
35. Fernández-Ruiz J., García C., Sagredo O., Gómez-Ruiz M., de Lago E. The endocannabinoid system as a target for the treatment of neuronal damage. Expert Opin. Ther. Targets 2010, 14:387-404.
36. 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.
37. Fondell E., O'Reilly E.J., Fitzgerald K.C., Falcone G.J., McCullough M.L., Park Y., et al. Magnesium intake and risk of amyotrophic lateral sclerosis: results from five large cohort studies. Amyotroph. Lateral Scler. Frontotemporal Degener. 2013, 14:356-361.
38. Foran E., Trotti D. Glutamate transporters and the excitotoxic path to motor neuron degeneration in amyotrophic lateral sclerosis. Antioxid. Redox Signal 2009, 11:1587-1602.
39. 9-THC (marinol) treatment for ALS. Amyotroph. Lateral Scler. Other Motor Neuron Disord. 2002, 3:23.
40. Gendron T.F., Belzil V.V., Zhang Y.J., Petrucelli L. Mechanisms of toxicity in C9FTLD/ALS. Acta Neuropathol. 2014, 127:359-376.
41. Giordana M.T., Piccinini M., Grifoni S., De Marco G., Vercellino M., Magistrello M., et al. TDP-43 redistribution is an early event in sporadic amyotrophic lateral sclerosis. Brain Pathol. 2010, 20:351-360.
42. Glass J.D. New drugs for ALS: how do we get there?. Exp. Neurol. 2012, 233:112-117.
43. Groen E.J., van Es M.A., van Vught P.W., Spliet W.G., van Engelen-Lee J., de Visser M., et al. FUS mutations in familial amyotrophic lateral sclerosis in the Netherlands. Arch. Neurol. 2010, 67:224-230.
44. Habib A.A., Mitsumoto H. Emerging drugs for amyotrophic lateral sclerosis. Expert Opin. Emerg. Drugs 2011, 16:537-558.
45. Hardiman O., van den Berg L.H., Kiernan M.C. Clinical diagnosis and management of amyotrophic lateral sclerosis. Nat. Rev. Neurol. 2011, 7:639-649.
46. Harraz M.M., Marden J.J., Zhou W., Zhang Y., Williams A., Sharov V.S., et al. SOD1 mutations disrupt redox-sensitive Rac regulation of NADPH oxidase in a familial ALS model. J. Clin. Invest. 2008, 118:659-670.
47. Henkel J.S., Engelhardt J.I., Siklós L., Simpson E.P., Kim S.H., Pan T., et al. Presence of dendritic cells, MCP-1, and activated microglia/macrophages in amyotrophic lateral sclerosis spinal cord tissue. Ann. Neurol. 2004, 55:221-235.
48. Hensley K., Abdel-Moaty H., Hunter J., Mhatre M., Mou S., Nguyen K., et al. Primary glia expressing the G93A-SOD1 mutation present a neuroinflammatory phenotype and provide a cellular system for studies of glial inflammation. J. Neuroinflammation 2006, 3:2.
49. Hetz C., Thielen P., Matus S., Nassif M., Court F., Kiffin R., et al. XBP-1 deficiency in the nervous system protects against amyotrophic lateral sclerosis by increasing autophagy. Genes Dev. 2009, 23:2294-2306.
50. Ince P.G., Shaw P.J., Slade J.Y., Jones C., Hudgson P. Familial amyotrophic lateral sclerosis with a mutation in exon 4 of the Cu/Zn superoxide dismutase gene: pathological and immunocytochemical changes. Acta Neuropathol. 1996, 92:395-403.
51. Ito D., Seki M., Tsunoda Y., Uchiyama H., Suzuki N. Nuclear transport impairment of amyotrophic lateral sclerosis-linked mutations in FUS/TLS. Ann. Neurol. 2011, 69:152-162.
52. Janssens J., Van Broeckhoven C. Pathological mechanisms underlying TDP-43 driven neurodegeneration in FTLD-ALS spectrum disorders. Hum. Mol. Genet. 2013, 22:R77-R87.
53. Joerger M., Wilkins J., Fagagnini S., Baldinger R., Brenneisen R., Schneider U., et al. Single-dose pharmacokinetics and tolerability of oral δ9-tetrahydrocannabinol in patients with amyotrophic lateral sclerosis. Drug Metab. Lett. 2012, 6:102-108.
54. Joyce P.I., Fratta P., Fisher E.M., Acevedo-Arozena A. SOD1 and TDP-43 animal models of amyotrophic lateral sclerosis: recent advances in understanding disease toward the development of clinical treatments. Mamm. Genome 2011, 22:420-448.
55. Kiaei M., Kipiani K., Chen J., Calingasan N.Y., Beal M.F. Peroxisome proliferator-activated receptor-gamma agonist extends survival in transgenic mouse model of amyotrophic lateral sclerosis. Exp. Neurol. 2005, 191:331-336.
56. Kim K., Moore D.H., Makriyannis A., Abood M.E. AM1241, a cannabinoid CB2 receptor selective compound, delays disease progression in a mouse model of amyotrophic lateral sclerosis. Eur. J. Pharmacol. 2006, 542:100-105.
57. King A.E., Dickson T.C., Blizzard C.A., Foster S.S., Chung R.S., West A.K., et al. Excitotoxicity mediated by non-NMDA receptors causes distal axonopathy in long-term cultured spinal motor neurons. Eur. J. Neurosci. 2007, 26:2151-2159.
58. Kirby J., Halligan E., Baptista M.J., Allen S., Heath P.R., Holden H., et al. Mutant SOD1 alters the motor neuronal transcriptome: implications for familial ALS. Brain 2005, 128:1686-1706.
59. Körner S., Kollewe K., Ilsemann J., Müller-Heine A., Dengler R., Krampfl K., et al. Prevalence and prognostic impact of comorbidities in amyotrophic lateral sclerosis. Eur. J. Neurol. 2013, 20:647-654.
60. Kuhle J., Lindberg R.L., Regeniter A., Mehling M., Steck A.J., Kappos L., et al. Increased levels of inflammatory chemokines in amyotrophic lateral sclerosis. Eur. J. Neurol. 2009, 16:771-774.
61. Lacomblez L., Bensimon G., Leigh P.N., Guillet P., Meininger V. Dose-ranging study of riluzole in amyotrophic lateral sclerosis. Amyotrophic Lateral Sclerosis/Riluzole Study Group II. Lancet 1996, 347:1425-1431.
62. Lagier-Tourenne C., Polymenidou M., Cleveland D.W. TDP-43 and FUS/TLS: emerging roles in RNA processing and neurodegeneration. Hum. Mol. Genet. 2010, 19:R46-R64.
63. Limousin N., Blasco H., Corcia P., Gordon P.H., De Toffol B., Andres C., et al. Malnutrition at the time of diagnosis is associated with a shorter disease duration in ALS. J. Neurol. Sci. 2010, 297:36-39.
64. Liscic R.M., Breljak D. Molecular basis of amyotrophic lateral sclerosis. Prog. Neuropsychopharmacol. Biol. Psychiatry 2011, 35:370-372.
65. Liu-Yesucevitz L., Bilgutay A., Zhang Y.J., Vanderweyde T., Citro A., Mehta T., et al. Tar DNA binding protein-43 (TDP-43) associates with stress granules: analysis of cultured cells and pathological brain tissue. PLOS ONE 2010, 5:e13250.
66. Ludolph A.C., Bendotti C., Blaugrund E., Chio A., Greensmith L., Loeffler J.P., et al. Guidelines for preclinical animal research in ALS/MND: a consensus meeting. Amyotroph. Lateral Scler. 2010, 11:38-45.
67. Mackenzie I.R., Rademakers R., Neumann M. TDP-43 and FUS in amyotrophic lateral sclerosis and frontotemporal dementia. Lancet Neurol. 2010, 9:995-1007.
68. Mantovani S., Garbelli S., Pasini A., Alimonti D., Perotti C., Melazzini M., et al. Immune system alterations in sporadic amyotrophic lateral sclerosis patients suggest an ongoing neuroinflammatory process. J. Neuroimmunol. 2009, 210:73-79.
69. Marchetto M.C., Muotri A.R., Mu Y., Smith A.M., Cezar G.G., Gage F.H. Non-cell-autonomous effect of human SOD1 G37R astrocytes on motor neurons derived from human embryonic stem cells. Cell Stem Cell 2008, 3:649-657.
70. Marden J.J., Harraz M.M., Williams A.J., Nelson K., Luo M., Paulson H., et al. Redox modifier genes in amyotrophic lateral sclerosis in mice. J. Clin. Invest. 2007, 117:2913-2919.
71. Martin L.J. Mitochondrial pathobiology in ALS. J. Bioenerg. Biomembr. 2011, 43:569-579.
72. Mattiazzi M., D'Aurelio M., Gajewski C.D., Martushova K., Kiaei M., Beal M.F., et al. Mutated human SOD1 causes dysfunction of oxidative phosphorylation in mitochondria of transgenic mice. J. Biol. Chem. 2002, 277:29626-29633.
73. Mitchell J., Paul P., Chen H.J., Morris A., Payling M., Falchi M., et al. Familial amyotrophic lateral sclerosis is associated with a mutation in D-amino acid oxidase. Proc. Natl Acad. Sci. USA 2010, 107:7556-7561.
74. Mitsumoto H., Santella R.M., Liu X., Bogdanov M., Zipprich J., Wu H.C., et al. Oxidative stress biomarkers in sporadic ALS. Amyotroph. Lateral Scler. 2008, 9:177-183.
75. Moreno-Martet M., Mestre L., Loría F., Guaza C., Fernández-Ruiz J., de Lago E. Identification of receptors and enzymes for endocannabinoids in NSC-34 cells: relevance for in vitro studies with cannabinoids in motor neuron diseases. Neurosci. Lett. 2012, 508:67-72.
76. Moreno-Martet M., Espejo-Porras F., Fernández-Ruiz J., de Lago E. Changes in endocannabinoid receptors and enzymes in the spinal cord of SOD1(G93A) transgenic mice and evaluation of a Sativex®-like combination of phytocannabinoids: interest for future therapies in amyotrophic lateral sclerosis. CNS Neurosci. Ther. 2014, 20:809-815.
77. Muyderman H., Hutson P.G., Matusica D., Rogers M.L., Rush R.A. The human G93A-superoxide dismutase-1 mutation, mitochondrial glutathione and apoptotic cell death. Neurochem. Res. 2009, 34:1847-1856.
78. Neumann M., Sampathu D.M., Kwong L.K., Truax A.C., Micsenyi M.C., Chou T.T., et al. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 2006, 314:130-133.
79. Neymotin A., Calingasan N.Y., Wille E., Naseri N., Petri S., Damiano M., et al. Neuroprotective effect of Nrf2/ARE activators, CDDO ethylamide and CDDO trifluoroethylamide, in a mouse model of amyotrophic lateral sclerosis. Free Radic. Biol. Med. 2011, 51:88-96.
80. Nishitoh H., Kadowaki H., Nagai A., Maruyama T., Yokota T., Fukutomi H., et al. ALS-linked mutant SOD1 induces ER stress- and ASK1-dependent motor neuron death by targeting Derlin-1. Genes Dev. 2008, 22:1451-1464.
81. Orrell R.W., Lane R.J., Ross M. Antioxidant treatment for amyotrophic lateral sclerosis/motor neuron disease. Cochrane Database Syst. Rev. 2007 2007, 1. CD002829.
82. Parakh S., Spencer D.M., Halloran M.A., Soo K.Y., Atkin J.D. Redox regulation in amyotrophic lateral sclerosis. Oxid. Med. Cell. Longev. 2013, 2013:408681.
83. Park S.W., Yi J.H., Miranpuri G., Satriotomo I., Bowen K., Resnick D.K., et al. Thiazolidinedione class of peroxisome proliferator-activated receptor gamma agonists prevents neuronal damage, motor dysfunction, myelin loss, neuropathic pain, and inflammation after spinal cord injury in adult rats. J. Pharmacol. Exp. Ther. 2007, 320:1002-1012.
84. Parkinson N., Ince P.G., Smith M.O., Highley R., Skibinski G., Andersen P.M., et al. ALS phenotypes with mutations in CHMP2B (charged multivesicular body protein 2B). Neurology 2006, 67:1074-1077.
85. Pascuzzi R.M., Shefner J., Chappell A.S., Bjerke J.S., Tamura R., Chaudhry V., et al. A phase II trial of talampanel in subjects with amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. 2010, 11:266-271.
86. Phukan J., Elamin M., Bede P., Jordan N., Gallagher L., Byrne S., et al. The syndrome of cognitive impairment in amyotrophic lateral sclerosis: a population-based study. J. Neurol. Neurosurg. Psychiatry 2012, 83:102-108.
87. Popat R.A., Tanner C.M., van den Eeden S.K., Bernstein A.L., Bloch D.A., Leimpeter A., et al. Effect of non-steroidal anti-inflammatory medications on the risk of amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. 2007, 8:157-163.
88. Raman C., McAllister S.D., Rizvi G., Patel S.G., Moore D.H., Abood M.E. Amyotrophic lateral sclerosis: delayed disease progression in mice by treatment with a cannabinoid. Amyotroph. Lateral Scler. Other Motor Neuron Disord. 2004, 5:33-39.
89. Renton A.E., Majounie E., Waite A., Simón-Sánchez J., Rollinson S., Gibbs J.R., et al. A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 2011, 72:257-268.
90. Renton A.E., Chiò A., Traynor B.J. State of play in amyotrophic lateral sclerosis genetics, 2014. Nat. Neurosci. 2014, 17:17-23.
91. 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, 362:59-62.
92. Rossi S., Bernardi G., Centonze D. The endocannabinoid system in the inflammatory and neurodegenerative processes of multiple sclerosis and of amyotrophic lateral sclerosis. Exp. Neurol. 2010, 224:92-102.
93. Rothstein J.D., Patel S., Regan M.R., Haenggeli C., Huang Y.H., Bergles D.E., et al. β-Lactam antibiotics offer neuroprotection by increasing glutamate transporter expression. Nature 2005, 433:73-77.
94. Salazar M., Carracedo A., Salanueva I.J., Hernández-Tiedra S., Lorente M., Egia A., et al. Cannabinoid action induces autophagy-mediated cell death through stimulation of ER stress in human glioma cells. J. Clin. Invest. 2009, 119:1359-1372.
95. Sargsyan S.A., Monk P.N., Shaw P.J. Microglia as potential contributors to motor neuron injury in amyotrophic lateral sclerosis. Glia 2005, 51:241-253.
96. Saxena S., Cabuy E., Caroni P. A role for motoneuron subtype-selective ER stress in disease manifestations of FALS mice. Nat. Neurosci. 2009, 12:627-636.
97. Schütz B., Reimann J., Dumitrescu-Ozimek L., Kappes-Horn K., Landreth G.E., Schürmann B., et al. The oral antidiabetic pioglitazone protects from neurodegeneration and amyotrophic lateral sclerosis-like symptoms in superoxide dismutase-G93A transgenic mice. J. Neurosci. 2005, 25:7805-7812.
98. Shaw P.J., Forrest V., Ince P.G., Richardson J.P., Wastell H.J. CSF and plasma amino acid levels in motor neuron disease: elevation of CSF glutamate in a subset of patients. Neurodegeneration 1995, 4:209-216.
99. Shibata N., Hirano A., Kobayashi M., Sasaki S., Kato T., Matsumoto S., et al. Cu/Zn superoxide dismutase-like immunoreactivity in Lewy body-like inclusions of sporadic amyotrophic lateral sclerosis. Neurosci. Lett. 1994, 179:149-152.
100. Shoemaker J.L., Seely K.A., Reed R.L., Crow J.P., Prather P.L. 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.
101. Siciliano G., Carlesi C., Pasquali L., Piazza S., Pietracupa S., Fornai F., et al. Clinical trials for neuroprotection in ALS. CNS Neurol. Disord. Drug Targets 2010, 9:305-313.
102. Sreedharan J., Blair I.P., Tripathi V.B., Hu X., Vance C., Rogelj B., et al. TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science 2008, 319:1668-1672.
103. Strong M.J. The evidence for altered RNA metabolism in amyotrophic lateral sclerosis (ALS). J. Neurol. Sci. 2010, 288:1-12.
104. Swarup V., Phaneuf D., Dupré N., Petri S., Strong M., Kriz J., et al. Deregulation of TDP-43 in amyotrophic lateral sclerosis triggers nuclear factor κB-mediated pathogenic pathways. J. Exp. Med. 2011, 208:2429-2447.
105. Turner M.R., Cagnin A., Turkheimer F.E., Miller C.C., Shaw C.E., Brooks D.J., et al. Evidence of widespread cerebral microglial activation in amyotrophic lateral sclerosis: an [11C](R)-PK11195 positron emission tomography study. Neurobiol. Dis. 2004, 15:601-609.
106. Van Hoecke A., Schoonaert L., Lemmens R., Timmers M., Staats K.A., Laird A.S., et al. EPHA4 is a disease modifier of amyotrophic lateral sclerosis in animal models and in humans. Nat. Med. 2012, 18:1418-1422.
107. Van Langenhove T., van der Zee J., Van Broeckhoven C. The molecular basis of the frontotemporal lobar degeneration-amyotrophic lateral sclerosis spectrum. Ann. Med. 2012, 44:817-828.
108. Vargas M.R., Johnson D.A., Sirkis D.W., Messing A., Johnson J.A. Nrf2 activation in astrocytes protects against neurodegeneration in mouse models of familial amyotrophic lateral sclerosis. J. Neurosci. 2012, 28:13574-13581.
109. Vijayalakshmi K., Alladi P.A., Ghosh S., Prasanna V.K., Sagar B.C., Nalini A., et al. Evidence of endoplasmic reticular stress in the spinal motor neurons exposed to CSF from sporadic amyotrophic lateral sclerosis patients. Neurobiol. Dis. 2011, 41:695-705.
110. Wang H., O'Reilly É.J., Weisskopf M.G., Logroscino G., McCullough M.L., Schatzkin A., et al. Vitamin E intake and risk of amyotrophic lateral sclerosis: a pooled analysis of data from 5 prospective cohort studies. Am. J. Epidemiol. 2011, 173:595-602.
111. Weber M., Goldman B., Truniger S. Tetrahydrocannabinol (THC) for cramps in amyotrophic lateral sclerosis: a randomised, double-blind crossover trial. J. Neurol. Neurosurg. Psychiatry 2010, 81:1135-1140.
112. Wegorzewska I., Baloh R.H. TDP-43-based animal models of neurodegeneration: new insights into ALS pathology and pathophysiology. Neurodegener. Dis. 2011, 8:262-274.
113. 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, 6:182-184.
114. Wiedemann F.R., Manfredi G., Mawrin C., Beal M.F., Schon E.A. Mitochondrial DNA and respiratory chain function in spinal cords of ALS patients. J. Neurochem. 2002, 80:616-625.
115. 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, 89:1555-1557.
116. Wong P.C., Pardo C.A., Borchelt D.R., Lee M.K., Copeland N.G., Jenkins N.A., et al. An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron 1995, 14:1105-1116.
117. Wright S. Cannabinoid-based medicines for neurological disorders-clinical evidence. Mol. Neurobiol. 2007, 36:129-136.
118. Wu L.S., Cheng W.C., Shen C.K. Targeted depletion of TDP-43 expression in the spinal cord motor neurons leads to the development of amyotrophic lateral sclerosis-like phenotypes in mice. J. Biol. Chem. 2012, 287:27335-27344.
119. Yamagishi S., Koyama Y., Katayama T., Taniguchi M., Hitomi J., Kato M., et al. An in vitro model for Lewy body-like hyaline inclusion/astrocytic hyaline inclusion: induction by ER stress with an ALS-linked SOD1 mutation. PLOS ONE 2007, 2:e1030.
120. 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.
121. Yamashita S., Mori A., Kimura E., Mita S., Maeda Y., Hirano T., et al. DJ-1 forms complexes with mutant SOD1 and ameliorates its toxicity. J. Neurochem. 2010, 113:860-870.
122. Yiangou Y., Facer P., Durrenberger P., Chessell I.P., Naylor A., Bountra C., et al. COX-2, CB2 and P2X7-immunoreactivities are increased in activated microglial cells/macrophages of multiple sclerosis and amyotrophic lateral sclerosis spinal cord. BMC Neurol. 2006, 6:12.
123. Zhao P., Ignacio S., Beattie E.C., Abood M.E. Altered presymptomatic AMPA and cannabinoid receptor trafficking in motor neurons of ALS model mice: implications for excitotoxicity. Eur. J. Neurosci. 2008, 27:572-579.