New therapy options for amyotrophic lateral sclerosis

Expert Opinion on Pharmacotherapy

Volumn 14, Issue 14, 2013, Pages 1907-1917

  Gordon, Paul ^a   Corcia, Philippe ^b   Meininger, Vincent ^c  

^a Northern Navajo Medical Center   (United States)

^b CHU BRETONNEAU   (France)

^c PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

Amyotrophic lateral sclerosis; Clinical trials; Muscle; Stem cells

Indexed keywords

DNA BINDING PROTEIN; ISIS 33611; NEUROTROPHIC FACTOR; NOGO 66 RECEPTOR; NUCLEOTIDE; OZANEZUMAB; PLACEBO; PROTEIN NOGO A; RILUZOLE; TIRASEMTIV; UNCLASSIFIED DRUG; VASCULOTROPIN;

AMYOTROPHIC LATERAL SCLEROSIS; ANTISENSE THERAPY; BLOOD BRAIN BARRIER; BONE MARROW TRANSPLANTATION; DIETARY INTAKE; DOSE RESPONSE; DRUG BLOOD LEVEL; DRUG DOSE ESCALATION; DRUG INDUCED HEADACHE; DRUG SAFETY; DRUG TARGETING; DRUG TOLERABILITY; FITNESS; GENE EXPRESSION; GENE MUTATION; GENE TARGETING; GROWTH HORMONE RELEASE; HUMAN; MAXIMUM TOLERATED DOSE; MESENCHYMAL STEM CELL TRANSPLANTATION; MOTONEURON; MUSCLE BIOPSY; MUSCLE FUNCTION; MUSCLE STRENGTH; NERVE FIBER GROWTH; NEURAL STEM CELL TRANSPLANTATION; NEUROMUSCULAR SYNAPSE; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PATHOPHYSIOLOGY; PLURIPOTENT STEM CELL; POSTDURAL PUNCTURE HEADACHE; RATING SCALE; REVIEW; SIGNAL TRANSDUCTION; SINGLE DRUG DOSE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; GENE EXPRESSION REGULATION; HUMANS; MUSCLES; NUTRITION THERAPY; STEM CELL TRANSPLANTATION;

EID: 84884214946     PISSN: 14656566     EISSN: 17447666     Source Type: Journal    
DOI: 10.1517/14656566.2013.819344     Document Type: Review

References (98)

1. Gordon PH, Meininger V. How can we improve clinical trials in amyotrophic lateral sclerosis̈Nat Rev Neurol 2011;7:650-4
2. Benatar M. Lost in translation: Treatment trials in the SOD1 mouse and in human ALS. Neurobiol Dis 2007;26:1-13
3. Ludolph AC, Bendotti C, Blaugrund E, et al. Guidelines for preclinical animal research in ALS/MND: A consensus meeting. Amyotroph Lateral Scler 2010;11:38-45
4. Mitsumoto H, Gordon P, Kaufmann P, et al. Randomized control trials in ALS: Lessons learned. Amyotroph Lateral Scler Other Motor Neuron Disord 2004;5(Suppl1):8-13
5. Fischer LR, Culver DG, Tennant P, et al. Amyotrophic lateral sclerosis is a distal axonopathy: Evidence in mice and man. Exp Neurol 2004;185:232-40
6. Williams AH, Valdez G, Moresi V, et al. MicroRNA-206 delays ALS progression and promotes regeneration of neuromuscular synapses in mice. Science 2009;326(5959):1549-54
7. Dupuis L, Echaniz-Laguna A. Skeletal muscle in motor neuron diseases: Therapeutic target and delivery route for potential treatments. Curr Drug Targets 2010. [Epub ahead of print
8. Dupuis L, Loeffler JP. Neuromuscular junction destruction during amyotrophic lateral sclerosis: Insights from transgenic models. Curr Opin Pharmacol 2009;9:341-6
9. Dupuis L, Gonzalez de Aguilar JL, di Scala F, et al. Nogo provides a molecular marker for diagnosis of amyotrophic lateral sclerosis. Neurobiol Dis 2002;10:358-65
10. Wang T, Xiong JQ, Ren XB, et al. The role of Nogo-A in neuroregeneration: A review. Brain Res Bull 2012;87:499-503
11. Liu BP, Fournier A, GrandPre T, et al. Myelin-associated glycoprotein as a functional ligand for the Nogo-66 receptor. Science 2002;297:1190-3
12. Wang KC, Koprivica V, Kim JA, et al. Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature 2002;417:941-4
13. Wang X, Chun SJ, Treloar H, et al. Localization of Nogo-A and Nogo-66 receptor proteins at sites of axon-myelin and synaptic contact. J Neurosci 2002;22:5505-15
14. Venkatesh K, Chivatakarn O, Sheu SS, et al. Molecular dissection of the myelin-associated glycoprotein receptor complex reveals cell type-specific mechanisms for neurite outgrowth inhibition. J Cell Biol 2007;177:393-9
15. GrandPre T, Li S, Strittmatter SM. Nogo-66 receptor antagonist peptide promotes axonal regeneration. Nature 2002;417:547-51
16. Schwab ME. Nogo and axon regeneration. Curr Opin Neurobiol 2004;14:118-24
17. Jokic N, Aguilar JLG, Pradat PF, et al. Nogo expression in muscle correlates with amyotrophic lateral sclerosis severity. Ann Neurol 2005;57:553-6
18. Pradat PF, Bruneteau G, Gonzalez de Aguilar JL, et al. Muscle Nogo-A expression is a prognostic marker in lower motor neuron syndromes. Ann Neurol 2007;62:15-20
19. Jokic N, Gonzalez de Aguilar JL, Dimou L, et al. The neurite outgrowth inhibitor Nogo-A promotes denervation in an amyotrophic lateral sclerosis model. EMBO Rep 2006;7:1162-7
20. Wojcik S, Engel WK, Askanas V. Increased expression of Nogo-A in ALS muscle biopsies is not unique for this disease. Acta Myol 2006;25:116-18
21. TÄgerud S, Libelius R, Magnusson C. Muscle Nogo-A: A marker for amyotrophic lateral sclerosis or for denervation̈Ann Neurol 2007;62:676
22. Askanas V, Wojcik S, Engel WK. Expression of Nogo-A in human muscle fibers is not specific for amyotrophic lateral sclerosis. Ann Neurol 2007;62:676-7
23. Wojcik S, Engel WK, Yan R. NOGO is increased and binds to BACE1 in sporadic inclusion-body myositis and in A beta PP-overexpressing cultured human muscle fibers. Acta Neuropathol 2007;114:517-26
24. Walmsley AR, Mir AK. Targeting the Nogo-A signalling pathway to promote recovery following acute CNS injury. Curr Pharm Des 2007;13:2470-84
25. Pradat PF, Corse A, Shefner J, et al. A first time in human study in ALS patients with the anti Nogo A monoclonal antibody GSK. 1223249. Preliminary Results. Amyotroph Lateral Scler 2011;12(Suppl1):47-9
26. Hinken AC, Driscoll LC, Lee K, et al. The fast skeletal troponin activator, CK-2017357, reduces muscle fatigue in an in situ model of vascular insufficiency. Presented at the Second Annual Aging Muscle Symposium; 30 September 2010; San Francisco, CA
27. Hansen R, Saikali KG, Chou W, et al. CK-2017357, a novel activator of fast skeletal muscle, increases isometric force evoked by electrical stimulation of the anterior tibialis muscle in healthy male subjects. Presented at the 40th Annual Meeting of the Society for Neuroscience; 13 November 2010; San Diego, CA
28. Shefner J, Cedarbaum JM, Cudkowicz ME, et al. Safety, tolerability and pharmacodynamics of a skeletal muscle activator in amyotrophic lateral sclerosis. Amyotroph Lateral Scler 2012;13:430-8
29. Maragakis NJ. Stem cells and the ALS neurologist. Amyotroph Lateral Scler 2010;11:417-23
30. Pandya RS, Mao LL, Zhou EW, et al. Neuroprotection for amyotrophic lateral sclerosis: Role of stem cells, growth factors, and gene therapy. Cent Nerv Syst Agents Med Chem 2012;12:15-12
31. Ma DK, Bonaguidi MA, Ming GL, et al. Adult neural stem cells in the mammalian central nervous system. Cell Res 2009;19:672-82
32. Corti S, Locatelli F, Papadimitriou D, et al. Neural stem cells LewisX+ CXCR4+ modify disease progression in an amyotrophic lateral sclerosis model. Brain 2007;130:1289-305
33. Xu L, Yan J, Chen D, et al. Human neural stem cell grafts ameliorate motor neuron disease in SOD-1 transgenic rats. Transplantation 2006;82:865-75
34. Xu L, Ryugo DK, Pongstaporn T, et al. Human neural stem cell grafts in the spinal cord of SOD1 transgenic rats: Differentiation and structural integration into the segmental motor circuitry. J Comp Neurol 2009;514:297-309
35. Teng YD, Benn SC, Kalkanis SN, et al. Multimodal actions of neural stem cells in a mouse model of ALS: A meta-analysis. Sci Transl Med 2012;4:165-4
36. Glass JD, Boulis NM, Johe K, et al. Lumbar intraspinal injection of neural stem cels in patients with amyotrophic lateral sclerosis: Results of a phase I trial in 12 patients. Stem Cells 2012;1144-51
37. Zhou S. From bone to brain: Human skeletal stem cell therapy for stroke. Cent Nerv Syst Agents Med Chem 2011;11:157-63
38. Kim H, Kim HY, Choi MR, et al. Dose-dependent efficacy of ALS-human mesenchymal stem cells transplantation into cisterna magna in SOD1-G93A ALS mice. Neurosci Lett 2010;468:190-4
39. Boucherie C, Schäfer S, Lavand'homme P, et al. Chimerization of astroglial population in the lumbar spinal cord after mesenchymal stem cell transplantation prolongs survival in a rat model of amyotrophic lateral sclerosis. J Neurosci Res 2009;87:2034-46
40. Mazzini L, Ferrero I, Luparello V, et al. Mesenchymal stem cell transplantation in amyotrophic lateral sclerosis: A phase I clinical trial. Exp Neurol 2010;223:229-37
41. Karussis D, Kargeorgiou C, Vaknin-Dembinsky A, et al. Safety and immunological effects of mesenchymal stem cell transplantation in patients with multiple sclerosis and amyotrophic lateral sclerosis. Arch Neurol 2010;67:1187-94
42. Gamez J, Carmona F, Raguer N, et al. Cellular transplants in amyotrophic lateral sclerosis patients: An observational study. Cytotherapy 2010;12:669-77
43. Takahashi K, Tanabe K, Ohnuki M, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007;131:861-72
44. Lee H, Shamy GA, Elkabetz Y, et al. Directed differentiation and transplantation of human embryonic stem cell-derived motoneurons. Stem Cells 2007;25:1931-9
45. Di Giorgio FP, Carrasco MA, Siao MC, et al. Non-cell autonomous effect of glia on motor neurons in an embryonic stem cell-based ALS model. Nat Neurosci 2007;10:608-14
46. Wyatt TJ, Rossi SL, Siegenthaler MM, et al. Human motor neuron progenitor transplantation leads to endogenous neuronal sparing in 3 models of motor neuron loss. Stem Cells Int 2011;2011:207-30
47. Dimos JT, Rodolfa KT, Niakan KK, et al. Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 2008;321:1218-21
48. Karumbayaram S, Novitch BG, Patterson M, et al. Directed differentiation of human-induced pluripotent stem cells generates active motor neurons. Stem Cells 2009;27:806-11
49. Mitne-Neto M, Machado-Costa M, Marchetto MC, et al. Downregulation of VAPB expression in motor neurons derived from induced pluripotent stem cells of ALS8 patients. Hum Mol Genet 2011;20:3642-52
50. Mattis VB, Svendsen CN. Induced pluripotent stem cells: A new revolution for clinical neurologÿLancet Neurol 2011;10:383-94
51. Beers DR, Henkel JS, Xiao Q, et al. Wild-type microglia extend survival in PU.1 knockout mice with familial amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 2006;103:16021-6
52. Corti S, Locatelli F, Donadoni C, et al. Wild-type bone marrow cells ameliorate the phenotype of SOD1-G93A ALS mice and contribute to CNS, heart and skeletal muscle tissues. Brain 2004;127:2518-32
53. Ohnishi S, Ito H, Suzuki Y, et al. Intra-bone marrow-bone marrow transplantation slows disease progression and prolongs survival in G93A mutant SOD1 transgenic mice, an animal model mouse for amyotrophic lateral sclerosis. Brain Res 2009;1296:216-24
54. Pastor D, Viso-León MC, Jones J, et al. Comparative effects between bone marrow and mesenchymal stem cell transplantation in GDNF expression and motor function recovery in a motor neuron degenerative mouse model. Stem Cell Rev 2012;8:45-58
55. Deda H, Inci MC, Kürekçi AE, et al. Treatment of amyotrophic lateral sclerosis patients by autologous bone marrow-derived hematopoietic stem cell transplantation: A 1-year follow-up. Cytotherapy 2009;11:18-25
56. Blanquer M, Moraleda JM, Iniesta F, et al. Neurotrophic bone marrow cellular nests prevent spinal motoneuron degeneration in amyotrophic lateral sclerosis patients: A pilot safety study. Stem Cells 2012;30:1277-85
57. Mattson MP, Cutler RG, Camandola S. Energy intake and amyotrophic lateral sclerosis. Neuromolecular Med 2007;9:17-20
58. Scarmeas N, Shih T, Stern Y, et al. Premorbid weight, body mass, and varsity athletics in ALS. Neurology 2002;59:773-5
59. Dupuis L, Pradat PF, Ludolph A, et al. Energy metabolism in amyotrophic lateral sclerosis. Lancet Neurol 2011;10:75-82
60. Dupuis L, Oudart H, René F, et al. Evidence for defective energy homeostasis in amyotrophic lateral sclerosis: Benefit of a high-energy diet ina transgenic mouse model. PNAS 2004;101:11159-64
61. Hamadeh M, Rodriguez MC, Kaczor J, et al. Caloric restriction transiently improves motor performance but hastens clinical Onset of disease in the Cu/Zn-superoxide dismutase mutant G93a mouse. Muscle Nerve 2005;31:214-20
62. Desport JC, Preux PM, Truong TC, et al. Nutritional status is a prognostic factor for survival in ALS patients. Neurology 1999;53:1059-63
63. Mattsson P, Lönnstedt I, Nygren I, et al. Physical fitness, but not muscle strength, is a risk factor for death in amyotrophic lateral sclerosis at an early age. J Neurol Neurosurg Psychiatry 2012;83:390-4
64. Turner MR, Wotton C, Talbot K, et al. Cardiovascular fitness as a risk factor for amyotrophic lateral sclerosis: Indirect evidence from record linkage study. J Neurol Neurosurg Psychiatry 2012;83:395-8
65. Chio A, Mora G. Physical fitness and amyotrophic lateral sclerosis: Dangerous liaisons or common genetic pathways̈J Neurol Neurosurg Psychiatry 2012;83:389
66. Desport JC, Torny F, Lacoste M, et al. Hypermetabolism in ALS: Correlations with clinical and paraclinical parameters. Neurodegener Dis 2005;2:202-7
67. Funalot B, Desport JC, Sturtz F, et al. High metabolic level in patients with familial amyotrophic lateral sclerosis. Amyotroph Lateral Scler 2009;10:113-17
68. Dupuis L, Corcia P, Fergani A, et al. Dyslipidemia is a protective factor in amyotrophic lateral sclerosis. Neurology 2008;70:1004-9
69. Dedic SI, Stevic Z, Dedic V, et al. Is hyperlipidemia correlated with longer survival in patients with amyotrophic lateral sclerosis̈Neurol Res 2012;34:576-80
70. Paganoni S, Deng J, Jaffa M, et al. Body mass index, not dyslipidemia, is an independent predictor of survival in amyotrophic lateral sclerosis. Muscle Nerve 2011;44:20-4
71. Sutedja NA, van der Schouw YT, Fischer K, et al. Beneficial vascular risk profile is associated with amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry 2011;82:638-42
72. Chio A, Calvo A, Ilardi A, et al. Lower serum lipid levels are related to respiratory impairment in patients with ALS. Neurology 2009;73:1681-5
73. Yang JW, Kim SM, Kim HJ, et al. Hypolipidemia in patients with amyotrophic lateral sclerosis: A possible gender differencëJ Clin Neurol 2013;9:125-9
74. Andersen PM, Al-Chalabi A. Clinical genetics of amyotrophic lateral sclerosis: What do we really knoẅNat Rev Neurol 2011;7:603-15
75. Wu CH, Fallini C, Ticozzi N, et al. Mutations in the profilin 1 gene cause familial amyotrophic lateral sclerosis. Nature 2012;488:499-503
76. Camu W, Khoris J, Moulard B, et al. Genetics of familial ALS and consequences for diagnosis. French ALS Research Group. J Neurol Sci 1999;165:S21-6
77. Valdmanis PN, Daoud H, Dion PA, et al. Recent advances in the genetics of amyotrophic lateral sclerosis. Curr Neurol Neurosci Rep 2009;9:198-205
78. Corcia P, Valdmanis P, Millecamps S, et al. Phenotype and genotype analysis in amyotrophic lateral sclerosis with TARDBP gene mutations. Neurology 2012;78:1519-26
79. Millecamps S, Salachas F, Cazeneuve C, et al. SOD1, ANG, VAPB, TARDBP, and FUS mutations in familial amyotrophic lateral sclerosis: Genotype-phenotype correlations. J Med Genet 2010;48:554-60
80. Kwiatkowski TJ Jr., Bosco DA, Leclerc AL, et al. Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 2009;323:1205-8
81. Renton A, Majounie E, Waite A, et al. A Hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 2011;72:257-68
82. Byrne S, Elamin M, Bede P, et al. Cognitive and clinical characteristics of patients with amyotrophic lateral sclerosis carrying a C9orf72 repeat expansion: A population-based cohort study. Lancet Neurol 2012;11:232-40
83. Lesage S, Le Ber I, Condroyer C, et al. C9orf72 repeat expansions are a rare genetic cause of parkinsonism. Brain 2013;136:385-91
84. Lindquist SG, Duno M, Batbayli M, et al. Corticobasal and ataxia syndromes widen the spectrum of C9ORF72 hexanucleotide expansion disease. Clin Genet 2013;83:279-83
85. Corcia P, Mayeux-Portas V, Khoris J, et al. Amyotrophic lateral sclerosis. Abnormal SMN1 gene copy number is a susceptibility factor for amyotrophic lateral sclerosis. Ann Neurol 2002;51:243-6
86. Veldink JH, Kalmijn S, Van der Hout AH, et al. SMN genotypes producing less SMN protein increase susceptibility to and severity of sporadic ALS. Neurology 2005;65:820-5
87. van Es MA, van Vught PW, Blauw HM, et al. Genetic variation in DPP6 is associated with susceptibility to amyotrophic lateral sclerosis. Nat Genet 2008;40:29-31
88. Lambrechts D, Storkebaum E, Morimoto M, et al. VEGF is a modifier of amyotrophic lateral sclerosis in mice and humans and protects motoneurons against ischemic death. Nat Genet 2003;34:383-94
89. Southwell AL, Skotte NH, Bennett CF, et al. Antisense oligonucleotide therapeutics for inherited neurodegenerative diseases. Trends Mol Med 2012;18:634-43
90. Miller TM, Pestronk A, David W, et al. An antisense oligonucleotide against SOD1 delivered intrathecally for patients with SOD1 familial amyotrophic lateral sclerosis: A phase 1, randomized, first-in-man study. Lancet Neurol 2013;12:435-42
91. Winer L, Srinivasan D, Chun S, et al. SOD1 in cerebral spinal fluid as a pharmacodynamic marker for antisense oligonucleotide therapy. JAMA Neurol 2013;70:201-7
92. Dalbello-Haas V, Florence JM, Krivickas LS. Therapeutic exercise for people with amyotrophic lateral sclerosis or motor neuron disease. Cochrane Database Syst Rev 2008(2):CD005229
93. Sinaki M, Mulder DW. Rehabilitation techniques for patients with amyotrophic lateral sclerosis. Mayo Clin Proc 1978;53:173-8
94. Beghi E, Logroscino G, Chiò A, et al. Amyotrophic lateral sclerosis, physical exercise, trauma and sports: Results of a population-based pilot case-control study. Amyotroph Lateral Scler 2010;11:289-92
95. Ravits JM, La Spada AR. ALS motor phenotype heterogeneity, focality, and spread: Deconstructing motor neuron degeneration. Neurology 2009;73:805-11
96. Km HJ, Kim NC, Wang YD, et al. Mutations in prion-like domains in hnRNPA2B1 and hnRNPA1 cause multisystem proteinopathy and ALS. Nature 2013. [Epub ahead of print
97. Chew S, Kanji AG, Montes J, et al. Olfactory ensheathing glia injections in Beijing: Misleading patients with ALS. Amyotroph Lateral Scler 2007;8:314-16
98. Abukhalil F, Lam BL, Guy J. Visual observations of an American patient with Leber hereditary optic neuropathy after purported injections of stem cells in China. Arch Ophthalmol 2012;130:532-4