Moving forward in clinical trials for ALS: Motor neurons lead the way please

Drug Discovery Today

Volumn 19, Issue 4, 2014, Pages 441-449

  Genç, Bariş ^a   Özdinler, P Hande ^a,b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AEOL 10150; CEFTRIAXONE; CELECOXIB; DEXPRAMIPEXOLE; GLUTAMIC ACID; LENALIDOMIDE; LITHIUM; MANGANESE DERIVATIVE; MINOCYCLINE; NAKED DNA; NEUROTROPHIN; NORPHENAZONE; OMIGAPIL; PORPHYRIN DERIVATIVE; RAPAMYCIN; RECOMBINANT BRAIN DERIVED NEUROTROPHIC FACTOR; RECOMBINANT METHIONYL BRAIN DERIVED NEUROTROPHIC FACTOR; RECOMBINANT SOMATOMEDIN C; RILUZOLE; THALIDOMIDE; UNCLASSIFIED DRUG; VASCULOTROPIN; ZK 187638; NERVE GROWTH FACTOR;

AMYOTROPHIC LATERAL SCLEROSIS; APOPTOSIS; AUTOPHAGY; HUMAN; INFLAMMATION; LIFESPAN; LONG TERM CARE; MOTONEURON; NEUROPROTECTION; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PROTEIN FOLDING; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; ANIMAL; CLINICAL TRIAL (TOPIC); METABOLISM; MITOCHONDRION; PATHOPHYSIOLOGY; PHYSIOLOGY;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; CLINICAL TRIALS AS TOPIC; GLUTAMIC ACID; HUMANS; MITOCHONDRIA; MOTOR NEURONS; NERVE GROWTH FACTORS;

EID: 84899575748     PISSN: 13596446     EISSN: 18785832     Source Type: Journal    
DOI: 10.1016/j.drudis.2013.10.014     Document Type: Review

References (92)

1. D.R. Rosen et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis Nature 362 1993 59 62
2. M.E. Gurney et al. Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation Science 264 1994 1772 1775
3. M.E. Gurney The use of transgenic mouse models of amyotrophic lateral sclerosis in preclinical drug studies J. Neurol. Sci. 152 Suppl. 1 1997 S67 S73
4. A.C. Ludolph et al. Guidelines for preclinical animal research in ALS/MND: a consensus meeting Amyotroph. Lateral Scler. 11 2010 38 45
5. G. Bensimon et al. A controlled trial of riluzole in amyotrophic lateral sclerosis. ALS/Riluzole Study Group N. Engl. J. Med. 330 1994 585 591
6. L. Lacomblez et al. Dose-ranging study of riluzole in amyotrophic lateral sclerosis. Amyotrophic Lateral Sclerosis/Riluzole Study Group II Lancet 347 1996 1425 1431
7. S.C. Barber, and P.J. Shaw Oxidative stress in ALS: key role in motor neuron injury and therapeutic target Free Radic. Biol. Med. 48 2010 629 641
8. M. Benatar Lost in translation: treatment trials in the SOD1 mouse and in human ALS Neurobiol. Dis. 26 2007 1 13
9. D.A. Bosco, and J.E. Landers Genetic determinants of amyotrophic lateral sclerosis as therapeutic targets CNS Neurol. Disord. Drug Targets 9 2010 779 790
10. A.A. Habib, and H. Mitsumoto Emerging drugs for amyotrophic lateral sclerosis Expert Opin. Emerg. Drugs 16 2011 537 558
11. M. Kuzma-Kozakiewicz, and H. Kwiecinski New therapeutic targets for amyotrophic lateral sclerosis Expert Opin. Ther. Targets 15 2011 127 143
12. A.C. Pawlyk et al. Current nervous system related drug targets for the treatment of amyotrophic lateral sclerosis Curr. Pharm. Des. 16 2010 2053 2073
13. L. Zinman, and M. Cudkowicz Emerging targets and treatments in amyotrophic lateral sclerosis Lancet Neurol. 10 2011 481 490
14. E.Y. Son et al. Conversion of mouse and human fibroblasts into functional spinal motor neurons Cell Stem Cell 9 2011 205 218
15. R. Benmohamed et al. Identification of compounds protective against G93A SOD1 toxicity for the treatment of amyotrophic lateral sclerosis Amyotroph. Lat. Scler. 12 2011 87 96
16. N. Egawa et al. Drug screening for ALS using patient-specific induced pluripotent stem cells Sci. Transl. Med. 4 2012 145ra104
17. J. Sandoe, and K. Eggan Opportunities and challenges of pluripotent stem cell neurodegenerative disease models Nat. Neurosci. 16 2013 780 789
18. J.D. Berry, and M.E. Cudkowicz New considerations in the design of clinical trials for amyotrophic lateral sclerosis Clin. Investig. 1 2011 1375 1389
19. M.E. Cudkowicz et al. Toward more efficient clinical trials for amyotrophic lateral sclerosis Amyotroph. Lateral Scler. 11 2010 259 265
20. S. Boillee et al. ALS: a disease of motor neurons and their nonneuronal neighbors Neuron 52 2006 39 59
21. W. Robberecht, and T. Philips The changing scene of amyotrophic lateral sclerosis Nat. Rev. Neurosci. 14 2013 248 264
22. M. Cozzolino et al. Amyotrophic lateral sclerosis: new insights into underlying molecular mechanisms and opportunities for therapeutic intervention Antioxid. Redox Signal. 17 2012 1277 1330
23. D.B. Drachman et al. Cyclooxygenase 2 inhibition protects motor neurons and prolongs survival in a transgenic mouse model of ALS Ann. Neurol. 52 2002 771 778
24. M. Kiaei et al. Thalidomide and lenalidomide extend survival in a transgenic mouse model of amyotrophic lateral sclerosis J. Neurosci. 26 2006 2467 2473
25. J. Kriz et al. Minocycline slows disease progression in a mouse model of amyotrophic lateral sclerosis Neurobiol. Dis. 10 2002 268 278
26. L. Van Den Bosch et al. Minocycline delays disease onset and mortality in a transgenic model of ALS Neuroreport 13 2002 1067 1070
27. M.E. Gurney et al. Riluzole preserves motor function in a transgenic model of familial amyotrophic lateral sclerosis Neurology 50 1998 62 66
28. J.D. Rothstein et al. Beta-lactam antibiotics offer neuroprotection by increasing glutamate transporter expression Nature 433 2005 73 77
29. B. Kalmar et al. Late stage treatment with arimoclomol delays disease progression and prevents protein aggregation in the SOD1 mouse model of ALS J. Neurochem. 107 2008 339 350
30. D. Kieran et al. Treatment with arimoclomol, a coinducer of heat shock proteins, delays disease progression in ALS mice Nat. Med. 10 2004 402 405
31. J.P. Crow et al. Manganese porphyrin given at symptom onset markedly extends survival of ALS mice Ann. Neurol. 58 2005 258 265
32. H. Ito et al. Treatment with edaravone, initiated at symptom onset, slows motor decline and decreases SOD1 deposition in ALS mice Exp. Neurol. 213 2008 448 455
33. S. Petri et al. Additive neuroprotective effects of a histone deacetylase inhibitor and a catalytic antioxidant in a transgenic mouse model of amyotrophic lateral sclerosis Neurobiol. Dis. 22 2006 40 49
34. M. Otto et al. Roadmap and standard operating procedures for biobanking and discovery of neurochemical markers in ALS Amyotroph. Lateral Scler. 13 2012 1 10
35. R. Bowser et al. Biomarkers in amyotrophic lateral sclerosis: opportunities and limitations Nat. Rev. Neurol. 7 2011 631 638
36. G93A transgenic ALS mice J. Neurosci. 31 2011 4166 4177
37. M.V. Yasvoina et al. eGFP expression under UCHL1 promoter genetically labels corticospinal motor neurons and a subpopulation of degeneration-resistant spinal motor neurons in an ALS mouse model J. Neurosci. 33 2013 7890 7904
38. J.B. Levine et al. Astrocytes interact intimately with degenerating motor neurons in mouse amyotrophic lateral sclerosis (ALS) Glia 28 1999 215 224
39. P.H. Gordon, and V. Meininger How can we improve clinical trials in amyotrophic lateral sclerosis? Nat. Rev. Neurol. 7 2011 650 654
40. B.K. Kaspar et al. Retrograde viral delivery of IGF-1 prolongs survival in a mouse ALS model Science 301 2003 839 842
41. B.K. Kaspar et al. Synergy of insulin-like growth factor-1 and exercise in amyotrophic lateral sclerosis Ann. Neurol. 57 2005 649 655
42. A.M. Vincent et al. IGF-I prevents glutamate-induced motor neuron programmed cell death Neurobiol. Dis. 16 2004 407 416
43. P.H. Ozdinler, and J.D. Macklis IGF-I specifically enhances axon outgrowth of corticospinal motor neurons Nat. Neurosci. 9 2006 1371 1381
44. E.C. Lai et al. Effect of recombinant human insulin-like growth factor-I on progression of ALS. A placebo-controlled study. The North America ALS/IGF-I Study Group Neurology 49 1997 1621 1630
45. G.D. Borasio et al. A placebo-controlled trial of insulin-like growth factor-I in amyotrophic lateral sclerosis. European ALS/IGF-I Study Group Neurology 51 1998 583 586
46. E.J. Sorenson et al. Subcutaneous IGF-1 is not beneficial in 2-year ALS trial Neurology 71 2008 1770 1775
47. W.G. Bradley et al. A Phase I/II study of recombinant human brain-derived neurotrophic factor in patients with amytrophic lateral sclerosis Ann. Neurol. 38 1995 971
48. the BDNF Study Group A controlled trial of recombinant methionyl human BDNF in ALS (Phase III) Neurology 52 1999 1427 1433
49. G. Ochs et al. A phase I/II trial of recombinant methionyl human brain derived neurotrophic factor administered by intrathecal infusion to patients with amyotrophic lateral sclerosis Amyotroph. Lateral Scler. Other Motor Neuron Disord. 1 2000 201 206
50. S. Kalra et al. A prospective, randomized, placebo-controlled evaluation of corticoneuronal response to intrathecal BDNF therapy in ALS using magnetic resonance spectroscopy: feasibility and results Amyotroph. Lateral Scler. Other Motor Neuron Disord. 4 2003 22 26
51. S. Park et al. Growth factor-expressing human neural progenitor cell grafts protect motor neurons but do not ameliorate motor performance and survival in ALS mice Exp. Mol. Med. 41 2009 487 500
52. A.C. Calvo et al. Lack of a synergistic effect of a non-viral ALS gene therapy based on BDNF and a TTC fusion molecule Orphanet. J. Rare Dis. 6 2011 10
53. M. Azzouz et al. VEGF delivery with retrogradely transported lentivector prolongs survival in a mouse ALS model Nature 429 2004 413 417
54. P. Klivenyi et al. Neuroprotective effects of creatine in a transgenic animal model of amyotrophic lateral sclerosis Nat. Med. 5 1999 347 350
55. R.J. Snow et al. Creatine supplementation and riluzole treatment provide similar beneficial effects in copper, zinc superoxide dismutase (G93A) transgenic mice Neuroscience 119 2003 661 667
56. G.J. Groeneveld et al. A randomized sequential trial of creatine in amyotrophic lateral sclerosis Ann. Neurol. 53 2003 437 445
57. J.M. Shefner et al. A clinical trial of creatine in ALS Neurology 63 2004 1656 1661
58. R. Danzeisen et al. Targeted antioxidative and neuroprotective properties of the dopamine agonist pramipexole and its nondopaminergic enantiomer SND919CL2x [(+)2-amino-4,5,6,7-tetrahydro-6-Lpropylamino-benzathiazole dihydrochloride] J. Pharmacol. Exp. Ther. 316 2006 189 199
59. M. Cudkowicz et al. The effects of dexpramipexole (KNS-760704) in individuals with amyotrophic lateral sclerosis Nat. Med. 17 2011 1652 1656
60. S.A. Rudnicki et al. Dexpramipexole effects on functional decline and survival in subjects with amyotrophic lateral sclerosis in a Phase II study: subgroup analysis of demographic and clinical characteristics Amyotroph. Lateral Scler. Frontotemporal Degener. 14 2013 44 51
61. H. Yoshino, and A. Kimura Investigation of the therapeutic effects of edaravone, a free radical scavenger, on amyotrophic lateral sclerosis (Phase II study) Amyotroph. Lateral Scler. 7 2006 241 245
62. R.W. Orrell AEOL-10150 (Aeolus) Curr. Opin. Investig. Drugs 7 2006 70 80
63. M.E. Cudkowicz et al. Arimoclomol at dosages up to 300 mg/day is well tolerated and safe in amyotrophic lateral sclerosis Muscle Nerve 38 2008 837 844
64. V. Lanka et al. Arimoclomol: a potential therapy under development for ALS Expert Opin. Investig. Drugs 18 2009 1907 1918
65. F. Fornai et al. Lithium delays progression of amyotrophic lateral sclerosis Proc. Natl. Acad. Sci. U. S. A. 105 2008 2052 2057
66. F. Fornai et al. Lithium in ALS: from the bench to the bedside Amyotroph. Lateral Scler. 9 2008 123 124
67. C. Pizzasegola et al. Treatment with lithium carbonate does not improve disease progression in two different strains of SOD1 mutant mice Amyotroph. Lateral Scler. 10 2009 221 228
68. A. Chio et al. Lithium carbonate in amyotrophic lateral sclerosis: lack of efficacy in a dose-finding trial Neurology 75 2010 619 625
69. S.P. Aggarwal et al. Safety and efficacy of lithium in combination with riluzole for treatment of amyotrophic lateral sclerosis: a randomised, double-blind, placebo-controlled trial Lancet Neurol. 9 2010 481 488
70. X. Zhang et al. Rapamycin treatment augments motor neuron degeneration in SOD1(G93A) mouse model of amyotrophic lateral sclerosis Autophagy 7 2011 412 425
71. I.F. Wang et al. Autophagy activators rescue and alleviate pathogenesis of a mouse model with proteinopathies of the TAR DNA-binding protein 43 Proc. Natl. Acad. Sci. U. S. A. 109 2012 15024 15029
72. G.J. Groeneveld et al. CGP 3466B has no effect on disease course of (G93A) mSOD1 transgenic mice Amyotroph. Lateral Scler. Other Motor Neuron Disord. 5 2004 220 225
73. R. Miller et al. Phase II/III randomized trial of TCH346 in patients with ALS Neurology 69 2007 776 784
74. H. Ryu et al. Sodium phenylbutyrate prolongs survival and regulates expression of anti-apoptotic genes in transgenic amyotrophic lateral sclerosis mice J. Neurochem. 93 2005 1087 1098
75. M. Li et al. Functional role of caspase-1 and caspase-3 in an ALS transgenic mouse model Science 288 2000 335 339
76. M.E. Cudkowicz et al. Trial of celecoxib in amyotrophic lateral sclerosis Ann. Neurol. 60 2006 22 31
77. A. Neymotin et al. Lenalidomide (Revlimid) administration at symptom onset is neuroprotective in a mouse model of amyotrophic lateral sclerosis Exp. Neurol. 220 2009 191 197
78. E.W. Stommel et al. Efficacy of thalidomide for the treatment of amyotrophic lateral sclerosis: a phase II open label clinical trial Amyotroph. Lateral Scler. 10 2009 393 404
79. A.F. Keller et al. Treatment with minocycline after disease onset alters astrocyte reactivity and increases microgliosis in SOD1 mutant mice Exp. Neurol. 228 2011 69 79
80. P.H. Gordon et al. Efficacy of minocycline in patients with amyotrophic lateral sclerosis: a phase III randomised trial Lancet Neurol. 6 2007 1045 1053
81. M. Tortarolo et al. Glutamate AMPA receptors change in motor neurons of SOD1G93A transgenic mice and their inhibition by a noncompetitive antagonist ameliorates the progression of amytrophic lateral sclerosis-like disease J. Neurosci. Res. 83 2006 134 146
82. M.C. Bellingham A review of the neural mechanisms of action and clinical efficiency of riluzole in treating amyotrophic lateral sclerosis: what have we learned in the last decade? CNS Neurosci. Ther. 17 2011 4 31
83. S. Scott et al. Design, power, and interpretation of studies in the standard murine model of ALS Amyotroph. Lateral Scler. 9 2008 4 15
84. H. Haddad et al. Riluzole attenuates spinal muscular atrophy disease progression in a mouse model Muscle Nerve 28 2003 432 437
85. T. Ishiyama et al. Riluzole slows the progression of neuromuscular dysfunction in the wobbler mouse motor neuron disease Brain Res. 1019 2004 226 236
86. P. Kennel et al. Riluzole prolongs survival and delays muscle strength deterioration in mice with progressive motor neuronopathy (pmn) J. Neurol. Sci. 180 2000 55 61
87. J. Seok et al. Genomic responses in mouse models poorly mimic human inflammatory diseases Proc. Natl. Acad. Sci. U. S. A. 110 2013 3507 3512
88. B.J. Molyneaux et al. Molecular development of corticospinal motor neuron circuitry Novartis Found. Symp. 288 2007 3 15 discussion 15-20, 96-18
89. R.N. Lemon Descending pathways in motor control Annu. Rev. Neurosci. 31 2008 195 218
90. Y. Kawamura et al. Morphometric comparison of the vulnerability of peripheral motor and sensory neurons in amyotrophic lateral sclerosis J. Neuropathol. Exp. Neurol. 40 1981 667 675
91. S.J. Del Signore et al. Combined riluzole and sodium phenylbutyrate therapy in transgenic amyotrophic lateral sclerosis mice Amyotroph. Lateral Scler. 10 2009 85 94
92. S. Waibel et al. Rasagiline alone and in combination with riluzole prolongs survival in an ALS mouse model J. Neurol. 251 2004 1080 1084