Mechanisms, models and biomarkers in amyotrophic lateral sclerosis

Amyotrophic Lateral Sclerosis and Frontotemporal Degeneration

Volumn 14, Issue SUPPL1, 2013, Pages 19-32

  Turner, Martin R ^a   Bowser, Robert ^b   Bruijn, Lucie ^c   Dupuis, Luc ^d,e   Ludolph, Albert ^e   McGrath, Michael ^f   Manfredi, Giovanni ^g   Maragakis, Nicholas ^h   Miller, Robert G ⁱ   Pullman, Seth L ^j   Rutkove, Seward B ^k   Shaw, Pamela J ^l   Shefner, Jeremy ^m   Fischbeck, Kenneth H ⁿ  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b BARROW NEUROLOGICAL INSTITUTE   (United States)

^c National Surgery Office   (United States)

^d UNIVERSITÉ DE STRASBOURG   (France)

^e UNIVERSITY OF ULM   (Germany)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g WEILL CORNELL MEDICAL COLLEGE   (United States)

^h JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

ⁱ CALIFORNIA PACIFIC MEDICAL CENTER   (United States)

^j Och Spine at New York Presbyterian Hospitals   (United States)

^k HARVARD MEDICAL SCHOOL   (United States)

^l UNIVERSITY OF SHEFFIELD   (United Kingdom)

^m State University of New York Upstate Medical University: College of Medicine   (United States)

ⁿ NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

more..

Author keywords

ALS; Biomarkers; Neuroimaging; Neurophysiology; Pathogenesis

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; BIOLOGICAL MARKER;

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; DISEASE ACTIVITY; ELECTROMYOGRAPHY; ENERGY METABOLISM; EXCITOTOXICITY; MOTONEURON; MOTOR UNIT; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OXIDATIVE STRESS; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; SKELETAL MUSCLE; SKIN; TRANSCRANIAL MAGNETIC STIMULATION; ANIMAL; DISEASE MODEL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; GENETICS; HUMAN; METABOLISM; NEUROIMAGING; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; BIOMARKERS; DISEASE MODELS, ANIMAL; HUMANS; MITOCHONDRIAL DISEASES; NEUROIMAGING; OXIDATIVE STRESS;

EID: 84877678524     PISSN: 21678421     EISSN: 21679223     Source Type: Journal    
DOI: 10.3109/21678421.2013.778554     Document Type: Article

References (148)

1. Kiernan MC, Vucic S, Cheah BC, Turner MR, Eisen A, Hardiman O, et al. Amyotroph Lateral Scler. Lancet. 2011; 377: 942-55.
2. Mackenzie IR, Bigio EH, Ince PG, Geser F, Neumann M, Cairns NJ, et al. Pathological TDP-43 distinguishes sporadic amyotrophic lateral sclerosis from amyotrophic lateral sclerosis with SOD1 mutations. Ann Neurol. 2007; 61: 427-34.
3. Mitchell JD, Callagher P, Gardham J, Mitchell C, Dixon M, Addison-Jones R, et al. Timelines in the diagnostic evaluation of people with suspected amyotrophic lateral sclerosis (ALS)/motor neuron disease (MND): a 20-year review. Can we do better? Amyotroph Lateral Scler. 2010; 11: 537-41.
4. Turner MR, Parton MJ, Shaw CE, Leigh PN, Al-Chalabi A. Prolonged survival in motor neuron disease: a descriptive study of the King's database 1990-2002. J Neurol Neurosurg Psychiatry. 2003; 74: 995-7.
5. Chio A, Calvo A, Moglia C, Mazzini L, Mora G. Pheno-typic heterogeneity of amyotrophic lateral sclerosis: a population based study. J Neurol Neurosurg Psychiatry. 2011; 82: 740-6.
6. Cudkowicz ME, Katz J, Moore DH, O'Neill G, Glass JD, Mitsumoto H, et al. Toward more effi cient clinical trials for amyotrophic lateral sclerosis. Amyotroph Lateral Scler. 2010; 11: 259-65.
7. Rothstein JD. Current hypotheses for the underlying biology of amyotrophic lateral sclerosis. Ann Neurol. 2009; 65 (Suppl 1): S3-9.
8. Rothstein JD, Tsai G, Kuncl RW, Clawson L, Cornblath DR, Drachman DB, et al. Abnormal excitatory amino acid metabolism in amyotrophic lateral sclerosis. Ann Neurol. 1990; 28: 18-25.
9. Spreux-Varoquaux O, Bensimon G, Lacomblez L, Salachas F, Pradat PF, Le Forestier N, et al. Glutamate levels in cerebrospinal fl uid in amyotrophic lateral sclerosis: a reappraisal using a new HPLC method with coulometric detection in a large cohort of patients. J NeurolvSci. 2002; 193: 73-8.
10. Rothstein JD, Dykes-Hoberg M, Pardo CA, Bristol LA, Jin L, Kuncl RW, et al. Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron. 1996; 16: 675-86.
11. Bruijn LI, Becher MW, Lee MK, Anderson KL, Jenkins NA, Copeland NG, et al. ALS-linked SOD1 mutant G85R mediates damage to astrocytes and promotes rapidly progressive disease with SOD1-containing inclusions. Neuron. 1997; 18: 327-38.
12. Howland DS, Liu J, She Y, Goad B, Maragakis NJ, Kim B, et al. Focal loss of the glutamate transporter EAAT2 in a transgenic rat model of SOD1 mutant-mediated amyo-trophic lateral sclerosis (ALS). Proc Natl Acad Sci U S A. 2002; 99: 1604-9.
13. 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.
14. Trotti D, Rolfs A, Danbolt NC, Brown RH Jr, Hediger MA. SOD1 mutants linked to amyotrophic lateral sclerosis selectively inactivate a glial glutamate transporter. Nat Neurosci. 1999; 2: 848.
15. Guo H, Lai L, Butchbach ME, Stockinger MP, Shan X, Bishop GA, et al. Increased expression of the glial glutamate transporter EAAT2 modulates excitotoxicity and delays the onset but not the outcome of ALS in mice. Hum Mol Genet. 2003; 12: 2519-32.
16. Rothstein JD, Patel S, Regan MR, Haenggeli C, Huang YH, Bergles DE, et al. Beta-lactam antibiotics offer neuroprotection by increasing glutamate transporter expression. Nature. 2005; 433: 73-7.
17. Doble A. The pharmacology and mechanism of action of riluzole. Neurology. 1996; 47 (Suppl 4): S233-41.
18. Turner MR, Kiernan MC. Does interneuronal dysfunction contribute to neurodegeneration in amytrophic lateral sclerosis? Amyotroph Lateral Scler. 2012; 13: 245-50.
19. Bogdanov M, Brown RH, Matson W, Smart R, Hayden D, O'Donnell H, et al. Increased oxidative damage to DNA in ALS patients. Free Radic Biol Med. 2000; 29: 652-8.
20. Simpson EP, Yen AA, Appel SH. Oxidative stress: a common denominator in the pathogenesis of amyotrophic lateral sclerosis. Current Opinion in Rheumatology. 2003; 15: 730-6. Epub 2003/10/22.
21. Barber SC, Shaw PJ. Oxidative stress in ALS: key role in motor neuron injury and therapeutic target. Free Radic Biol Med. 2010; 48: 629-41.
22. Turner MR, Kiernan MC, Leigh PN, Talbot K. Biomarkers in amyotrophic lateral sclerosis. Lancet Neurol. 2009; 8: 94-109.
23. Mitsumoto H, Santella RM, Liu X, Bogdanov M, Zipprich J, Wu HC, et al. Oxidative stress biomarkers in sporadic ALS. Amyotroph Lateral Scler. 2008; 9: 177-83.
24. Chang Y, Kong Q, Shan X, Tian G, Ilieva H, Cleveland DW, et al. Messenger RNA oxidation occurs early in disease pathogenesis and promotes motor neuron degeneration in ALS. PLoS One. 2008; 3: 2849.
25. Duan W, Li X, Shi J, Guo Y, Li Z, Li C. Mutant TAR DNA-binding protein-43 induces oxidative injury in motor neuron-like cell. Neuroscience. 2010; 169: 1621-9.
26. Kirby J, Halligan E, Baptista MJ, Allen S, Heath PR, Holden H, et al. Mutant SOD1 alters the motor neuronal transcriptome: implications for familial ALS. Brain. 2005; 128: 1686-706.
27. Harraz MM, Marden JJ, Zhou W, Zhang Y, Williams A, Sharov VS, et al. SOD1 mutations disrupt redox-sensitive Rac regulation of NADPH oxidase in a familial ALS model. J Clin Invest. 2008; 118: 659-70.
28. Sarlette A, Krampfl K, Grothe C, Neuhoff N, Dengler R, Petri S. Nuclear erythroid 2-related factor 2-antioxidative response element signaling pathway in motor cortex and spinal cord in amyotrophic lateral sclerosis. J Neuropathol Exp Neurol. 2008; 67: 1055-62.
29. Orrell RW, Lane RJ, Ross M. A systematic review of anti-oxidant treatment for amyotrophic lateral sclerosis/motor neuron disease. Amyotroph Lateral Scler. 2008; 9: 195-211.
30. Barber SC, Higginbottom A, Mead RJ, Barber S, Shaw PJ. An in vitro screening cascade to identify neuroprotective anti-oxidants in ALS. Free Radic Biol Med. 2009; 46: 1127-38.
31. Magrane J, Manfredi G. Mitochondrial function, morphology, and axonal transport in amyotrophic lateral sclerosis. Antioxid Redox Signal. 2009; 11: 1615-26.
32. Kawamata H, Manfredi G. Mitochondrial dysfunction and intracellular calcium dysregulation in ALS. Mech Ageing Dev. 2010; 131: 517-26.
33. Kawamata H, Manfredi G. Different regulation of wildtype and mutant Cu/Zn superoxide dismutase localization in mammalian mitochondria. Hum Mol Genet. 2008; 17: 3303-17.
34. Israelson A, Arbel N, Da Cruz S, Ilieva H, Yamanaka K, Shoshan-Barmatz V, et al. Misfolded mutant SOD1 directly inhibits VDAC1 conductance in a mouse model of inherited ALS. Neuron. 2010; 67: 575-87.
35. Li Q, van de Velde C, Israelson A, Xie J, Bailey AO, Dong MQ, et al. ALS-linked mutant superoxide dismutase-1 (SOD1) alters mitochondrial protein composition and decreases protein import. Proc Natl Acad Sci U S A. 2010; 107: 21146-51.
36. Pedrini S, Sau D, Guareschi S, Bogush M, Brown RH Jr, Naniche N, et al. ALS-linked mutant SOD1 damages mitochondria by promoting conformational changes in Bcl-2. Hum Mol Genet. 2010; 19: 2974-86.
37. van de Velde C, McDonald KK, Boukhedimi Y, McAlonis-Downes M, Lobsiger CS, Bel Hadj S, et al. Misfolded SOD1 associated with motor neuron mitochondria alters mitochondrial shape and distribution prior to clinical onset. PLoS One. 2011; 6: 22031.
38. Bordet T, Buisson B, Michaud M, Drouot C, Galea P, Delaage P, et al. Identifi cation and characterization of cholest-4-en-3-one, oxime (TRO19622), a novel drug candidate for amyotrophic lateral sclerosis. J Pharmacol Exp Ther. 2007; 322: 709-20.
39. Cudkowicz M, Bozik ME, Ingersoll EW, Miller R, Mitsumoto H, Shefner J, et al. The effects of dexpramipex-ole (KNS-760704) in individuals with amyotrophic lateral sclerosis. Nat Med. 2011; 17: 1652-6.
40. Alavian KN, Dworetzky SI, Bonanni L, Zhang P, Sacchetti S, Mariggio MA, et al. Effects of dexpramipexole on brain mitochondrial conductances and cellular bioener-getic effi ciency. Brain Res. 2012; 1446: 1-11.
41. Philips T, Robberecht W. Neuroinfl ammation in amyo-trophic lateral sclerosis: role of glial activation in motor neuron disease. Lancet Neurol. 2011; 10: 253-63.
42. Zhang R, Gascon R, Miller RG, Gelinas DF, Mass J, Hadlock K, et al. Evidence for systemic immune system alterations in sporadic amyotrophic lateral sclerosis (SALS). J Neuroimmunol. 2005; 159: 215-24. Epub 2005/01/18.
43. Mitchell RM, Freeman WM, Randazzo WT, Stephens HE, Beard JL, Simmons Z, et al. A CSF biomarker panel for identifi cation of patients with amyotrophic lateral sclerosis. Neurology. 2009; 72: 14-9.
44. Kuhle J, Lindberg RL, Regeniter A, Mehling M, Steck AJ, Kappos L, et al. Increased levels of infl ammatory chemok-ines in amyotrophic lateral sclerosis. Eur J Neurol. 2009; 16: 771-4.
45. Zhang R, Miller RG, Gascon R, Champion S, Katz J, Lancero M, et al. Circulating endotoxin and systemic immune activation in sporadic amyotrophic lateral sclerosis (SALS). J Neuroimmunol. 2009; 206: 121-4. Epub 2008/11/18.
46. Appel SH, Engelhardt JI, Henkel JS, Siklos L, Beers DR, Yen AA, et al. Hematopoietic stem cell transplantation in patients with sporadic amyotrophic lateral sclerosis. Neurology. 2008; 71: 1326-34. Epub 2008/10/22.
47. Dupuis L, Oudart H, Rene F, Gonzalez de Aguilar JL, Loeffl er JP. Evidence for defective energy homeostasis in amyotrophic lateral sclerosis: benefi t of a high-energy diet in a transgenic mouse model. Proc Natl Acad Sci U S A. 2004; 101: 11159-64.
48. Dupuis L, Pradat PF, Ludolph AC, Loeffl er JP. Energy metabolism in amyotrophic lateral sclerosis. Lancet Neurol. 2011; 10: 75-82.
49. Paganoni S, Deng J, Jaffa M, Cudkowicz ME, Wills AM. Body mass index, not dyslipidemia, is an independent predictor of survival in amyotrophic lateral sclerosis. Muscle Nerve. 2011; 44: 20-4. Epub 2011/05/25.
50. Marin B, Desport JC, Kajeu P, Jesus P, Nicolaud B, Nicol M, et al. Alteration of nutritional status at diagnosis is a prognostic factor for survival of amyotrophic lateral sclerosis patients. J Neurol Neurosurg Psychiatry. 2011; 82: 628-34. Epub 2010/11/26.
51. Dupuis L, Corcia P, Fergani A, Gonzalez de Aguilar JL, Bonnefont-Rousselot D, Bittar R, et al. Dyslipidemia is a protective factor in amyotrophic lateral sclerosis. Neurology. 2008; 70: 1004-9.
52. Dorst J, Kühnlein P, Hendrich C, Kassubek J, Sperfeld AD, Ludolph AC. Patients with elevated triglyceride and cholesterol serum levels have a prolonged survival in amyo-trophic lateral sclerosis. J Neurol. 2011; 258: 613-7.
53. Chio A, Calvo A, Ilardi A, Cavallo E, Moglia C, Mutani R, et al. Lower serum lipid levels are related to respiratory impairment in patients with ALS. Neurology. 2009; 73: 1681-5. Epub 2009/11/18.
54. Lawton KA, Cudkowicz ME, Brown MV, Alexander D, Caffrey R, Wulff JE, et al. Biochemical alterations associated with ALS. Amyotroph Lateral Scler. 2012; 13: 110-8.
55. Müller HP, Raudies F, Unrath A, Neumann H, Ludolph AC, Kassubek J. Quantifi cation of human body fat tissue percentage by MRI. NMR Biomed. 2011; 24: 17-24. Epub 2010/07/31.
56. Joyce PI, Fratta P, Fisher EM, 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: 420-48.
57. Gama Sosa MA, de Gasperi R, Elder GA. Modeling human neurodegenerative diseases in transgenic systems. Hum Genet. 2012; 131: 535-63.
58. 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.
59. Dimos JT, Rodolfa KT, Niakan KK, Weisenthal LM, Mitsumoto H, Chung W, et al. Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science. 2008; 321: 1218-21.
60. Bilican B, Serio A, Barmada SJ, Nishimura AL, Sullivan GJ, Carrasco M, et al. Mutant induced pluripotent stem cell lines recapitulate aspects of TDP-43 proteinopa-thies and reveal cell-specifi c vulnerability. Proc Natl Acad Sci U S A. 2012; 109: 5803-8.
61. Thomson SR, Wishart TM, Patani R, Chandran S, Gillingwater TH. Using induced pluripotent stem cells (iPSC) to model human neuromuscular connectivity: promise or reality? J Anat. 2012; 220: 122-30.
62. Hu S, Loo JA, Wong DT. Human body fl uid proteome analysis. Proteomics. 2006; 6: 6326-53.
63. Ryberg H, Bowser R. Protein biomarkers for amyo-trophic lateral sclerosis. Expert Rev Proteomics. 2008; 5: 249-62.
64. Ranganathan S, Williams E, Ganchev P, Gopalakrishnan V, Lacomis D, Urbinelli L, et al. Proteomic profi ling of cer-ebrospinal fl uid identifi es biomarkers for amyotrophic lateral sclerosis. J Neurochem. 2005; 95: 1461-71.
65. Blasco H, Corcia P, Moreau C, Veau S, Fournier C, Vourc'h P, et al. 1H-NMR-based metabolomic profi ling of CSF in early amyotrophic lateral sclerosis. PLoS One. 2010; 5: 13223.
66. Kumar A, Bala L, Kalita J, Misra UK, Singh RL, Khetrapal CL, et al. Metabolomic analysis of serum by (1) H NMR spectroscopy in amyotrophic lateral sclerosis. Clin Chim Acta. 2010; 411: 563-7.
67. Wuolikainen A, Moritz T, Marklund SL, Antti H, Andersen PM. Disease related changes in the cerebrospinal fl uid metabolome in amyotrophic lateral sclerosis detected by GC/TOFMS. PLoS One. 2011; 6: 17947.
68. Boylan K, Yang C, Crook J, Overstreet K, Heckman M, Wang Y, et al. Immunoreactivity of the phosphorylated axonal neurofi lament H subunit (pNF-H) in blood of ALS model rodents and ALS patients: evaluation of blood pNF-H as a potential ALS biomarker. J Neurochem. 2009; 111: 1182-91.
69. Brettschneider J, Petzold A, Submuth SD, Ludolph AC, Tumani H. Axonal damage markers in cerebrospinal fl uid are increased in ALS. Neurology. 2006; 66: 852-6.
70. Rosengren LE, Karlsson JE, Karlsson JO, Persson LI, Wikkelso C. Patients with amyotrophic lateral sclerosis and other neurodegenerative diseases have increased levels of neurofi lament protein in CSF. J Neurochem. 1996; 67: 2013-8.
71. Kasai T, Tokuda T, Ishigami N, Sasayama H, Foulds P, Mitchell DJ, et al. Increased TDP-43 protein in cerebros-pinal fl uid of patients with amyotrophic lateral sclerosis. Acta Neuropathol. 2009; 117: 55-62.
72. Steinacker P, Hendrich C, Sperfeld AD, Jesse S, von Arnim CA, Lehnert S, et al. TDP-43 in cerebrospinal fl uid of patients with frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Arch Neurol. 2008; 65: 1481-7.
73. Wilson ME, Boumaza I, Lacomis D, Bowser R. Cystatin C: a candidate biomarker for amyotrophic lateral sclerosis. PLoS One. 2011; 5: 15133.
74. Ganesalingam J, An J, Shaw CE, Shaw G, Lacomis D, Bowser R. Combination of neurofi lament heavy chain and complement C3 as CSF biomarkers for ALS. J Neurochem. 2011; 117: 528-37. Epub 2011/03/23.
75. Sussmuth SD, Sperfeld AD, Hinz A, Brettschneider J, Endruhn S, Ludolph AC, et al. CSF glial markers correlate with survival in amyotrophic lateral sclerosis. Neurology. 2010; 74: 982-7.
76. Wuolikainen A, Hedenstrom M, Moritz T, Marklund SL, Antti H, Andersen PM. Optimization of procedures for collecting and storing of CSF for studying the metabolome in ALS. Amyotroph Lateral Scler. 2009; 10: 229-36.
77. Otto M, Bowser R, Turner M, Berry J, Brettschneider J, Connor J, et al. Roadmap and standard operating procedures for biobanking and discovery of neurochemical markers in ALS. Amyotroph Lateral Scler. 2012; 13: 1-10.
78. Dupuis L, Gonzalez de Aguilar JL, di Scala F, Rene F, de Tapia M, Pradat PF, et al. Nogo provides a molecular marker for diagnosis of amyotrophic lateral sclerosis. Neurobiol Dis. 2002; 10: 358-65.
79. Jokic N, Gonzalez de Aguilar JL, Pradat PF, Dupuis L, Echaniz-Laguna A, Muller A, et al. Nogo expression in muscle correlates with amyotrophic lateral sclerosis severity. Ann Neurol. 2005; 57: 553-6.
80. Pradat PF, Bruneteau G, Gonzalez de Aguilar JL, Dupuis L, Jokic N, Salachas F, et al. Muscle Nogo-A expression is a prognostic marker in lower motor neuron syndromes. Ann Neurol. 2007; 62: 15-20.
81. Pradat PF, Dubourg O, de Tapia M, di Scala F, Dupuis L, Lenglet T, et al. Muscle gene expression is a marker of amyotrophic lateral sclerosis severity. Neurodegener Dis. 2012; 9: 38-52. Epub 2011/09/22.
82. Fang L, Teuchert M, Huber-Abel F, Schattauer D, Hendrich C, Dorst J, et al. MMP-2 and MMP-9 are elevated in spinal cord and skin in a mouse model of ALS. J Neurol Sci. 2010; 294: 51-6.
83. Fang L, Huber-Abel F, Teuchert M, Hendrich C, Dorst J, Schattauer D, et al. Linking neuron and skin: matrix metal-loproteinases in amyotrophic lateral sclerosis (ALS). J Neu-rol Sci. 2009; 285: 62-6.
84. Ono S. The skin in amyotrophic lateral sclerosis. Amyo-troph Lateral Scler Other Motor Neuron Disord. 2000; 1: 191-9.
85. Weis J, Katona I, Muller-Newen G, Sommer C, Necula G, Hendrich C, et al. Small-fi ber neuropathy in patients with ALS. Neurology. 2011; 76: 2024-9.
86. Haidet-Phillips AM, Hester ME, Miranda CJ, Meyer K, Braun L, Frakes A, et al. Astrocytes from familial and sporadic ALS patients are toxic to motor neurons. Nat Biotechnol. 2011; 29: 824-8.
87. Erminio F, Buchthal F, Rosenfalck P. Motor unit territory and muscle fi ber concentration in paresis due to peripheral nerve injury and anterior horn cell involvement. Neurology. 1959; 9: 657-71.
88. Shefner JM, Gooch CL. Motor unit number estimation. Phys Med Rehabil Clin N Am. 2003; 14: 243-60.
89. Shefner JM, Watson ML, Simionescu L, Caress JB, Burns TM, Maragakis NJ, et al. Multipoint incremental motor unit number estimation as an outcome measure in ALS. Neurology. 2011; 77: 235-41.
90. Nandedkar SD, Barkhaus PE, Stalberg EV. Reproducibility of MUNIX in patients with amyotrophic lateral sclerosis. Muscle Nerve. 2011; 44: 919-22.
91. Henderson RD, Ridall PG, Pettitt AN, McCombe PA. Results of Bayesian statistical analysis in normal and ALS subjects. Suppl Clin Neurophysiol. 2009; 60: 57-63.
92. Henderson RD, Ridall PG, Hutchinson NM, Pettitt AN, McCombe PA. Bayesian statistical MUNE method. Muscle Nerve. 2007; 36: 206-13.
93. Rossini PM, Rossi S. Transcranial magnetic stimulation: diagnostic, therapeutic, and research potential. Neurology. 2007; 68: 484-8.
94. Eisen A, Shytbel W, Murphy K, Hoirch M. Cortical magnetic stimulation in amyotrophic lateral sclerosis. Muscle Nerve. 1990; 13: 146-51.
95. Yokota T, Yoshino A, Inaba A, Saito Y. Double cortical stimulation in amyotrophic lateral sclerosis. J Neurol Neu-rosurg Psychiatry. 1996; 61: 596-600.
96. Weber M, Eisen A, Stewart HG, Andersen PM. Preserved slow conducting corticomotoneuronal projections in amyo-trophic lateral sclerosis with autosomal recessive D90A Cu/Zn superoxide dismutase mutation. Brain. 2000; 123: 1505-15.
97. Mitsumoto H, Ulug AM, Pullman SL, Gooch CL, Chan S, Tang MX, et al. Quantitative objective markers for upper and lower motor neuron dysfunction in ALS. Neurology. 2007; 68: 1402-10.
98. Attarian S, Vedel JP, Pouget J, Schmied A. Progression of cortical and spinal dysfunctions over time in amyotrophic lateral sclerosis. Muscle Nerve. 2008; 37: 364-75.
99. Floyd AG, Yu QP, Piboolnurak P, Tang MX, Fang Y, Smith W A, et al. Transcranial magnetic stimulation in ALS: utility of central motor conduction tests. Neurology. 2009; 72: 498-504.
100. Vucic S, Cheah BC, Yiannikas C, Kiernan MC. Cortical excitability distinguishes ALS from mimic disorders. Clin Neurophysiol. 2011; 122: 1860-6.
101. Rutkove SB. Electrical Impedance Myography: Background, Current State, and Future Directions. Muscle Nerve. 2009; 40: 936-46.
102. Rutkove SB, Zhang H, Schoenfeld DA, Raynor EM, Shefner JM, Cudkowicz ME, et al. Electrical impedance myography to assess outcome in amyotrophic lateral sclerosis clinical trials. Clin Neurophysiol. 2007; 118: 2413-8.
103. Rutkove SB, Caress JB, Cartwright MS, Burns TM, Warder J, David WS, et al. Electrical impedance myography as a biomarker to assess ALS progression. Amyotroph Lateral Scler. 2012; 13: 439-45.
104. Wang LL, Spieker AJ, Li J, Rutkove SB. Electrical impedance myography for monitoring motor neuron loss in the SOD1-G93A amyotrophic lateral sclerosis rat. Clinical neurophysiology: offi cial journal of the International Federation of Clinical Neurophysiology. 2011; 122: 2505-11. Epub 2011/05/27.
105. Glass JD, Boulis NM, Johe K, Rutkove SB, Federici T, Polak M, et al. Lumbar intraspinal injection of neural stem cells in patients with amyotrophic lateral sclerosis: results of a phase I trial in 12 patients. Stem Cells. 2012; 30: 1144-51. Epub 2012/03/15.
106. Ogunnika OT, Rutkove SB, Ma H, Fogerson PM, Scharfstein M, Cooper RC, et al. A portable system for the assessment of neuromuscular diseases with electrical impedance myography. Journal of Medical Engineering & Technology. 2010; 35: 377-85. Epub 2010/07/31.
107. Filippi M, Agosta F, Abrahams S, Fazekas F, Grosskreutz J, Kalra S, et al. EFNS guidelines on the use of neuroimaging in the management of motor neuron diseases. Eur J Neurol. 2010; 17:520-6.
108. Evans MC, Modo M, Talbot K, Sibson N, Turner MR. Magnetic resonance imaging of pathological processes in rodent models of amyotrophic lateral sclerosis. Amyotroph Lateral Scler. 2012; 13: 288-301.
109. Turner MR, Agosta F, Bede P, Govind V, Lule D, Verstraete E. Neuroimaging in amyotrophic lateral sclerosis. Biomark Med. 2012; 6: 319-37.
110. Neary D, Snowden JS, Mann DM, Northen B, Goulding PJ, Macdermott N. Frontal lobe dementia and motor neuron disease. J Neurol Neurosurg Psychiatry. 1990; 53: 23-32.
111. Kew JJ, Leigh PN, Playford ED, Passingham RE, Goldstein LH, Frackowiak RS, et al. Cortical function in amyotrophic lateral sclerosis: a positron emission tomography study. Brain. 1993; 116: 655-80.
112. Lloyd CM, Richardson MP, Brooks DJ, Al Chalabi A, Leigh PN. Extramotor involvement in ALS: PET studies with the GABA(A) ligand [(11)C]fl umazenil. Brain. 2000; 123: 2289-96.
113. Turner MR, Hammers A, Al-Chalabi A, Shaw CE, Andersen PM, Brooks DJ, et al. Distinct cerebral lesions in sporadic and D90A-SOD1 ALS: studies with [11C] fl umazenil PET. Brain. 2005; 128: 1323-9.
114. Turner MR, Cagnin A, Turkheimer FE, Miller CC, Shaw CE, Brooks DJ, et al. Evidence of widespread cerebral microglial activation in amyotrophic lateral sclerosis: an [(11)C](R)-PK11195 positron emission tomography study. Neurobiol Dis. 2004; 15: 601-9.
115. Turner MR, Rabiner EA, Hammers A, Al-Chalabi A, Grasby PM, Shaw CE, et al. [11C]-WAY100635 PET demonstrates marked 5-HT1A receptor changes in sporadic ALS. Brain. 2005; 128: 896-905.
116. Lanctot KL, Herrmann N, Ganjavi H, Black SE, Rusjan PM, Houle S, et al. Serotonin-1A receptors in fron-totemporal dementia compared with controls. Psychiatry Res. 2007; 156: 247-50.
117. Ding XQ, Kollewe K, Blum K, Korner S, Kehbel S, Dengler R, et al. Value of quantitative analysis of routine clinical MRI sequences in ALS. Amyotroph Lateral Scler. 2011; 12: 406-13.
118. Turner MR, Grosskreutz J, Kassubek J, Abrahams S, Agosta F, Benatar M, et al. Towards a neuroimaging biomarker for amyotrophic lateral sclerosis. Lancet Neurol. 2011; 10: 400-3.
119. Chen Z, Ma L. Grey matter volume changes over the whole brain in amyotrophic lateral sclerosis: a voxel-wise meta-analysis of voxel based morphometry studies. Amyotroph Lateral Scler. 2010; 11: 549-54.
120. Verstraete E, Veldink JH, Hendrikse J, Schelhaas HJ, van den Heuvel MP, van den Berg LH. Structural MRI reveals cortical thinning in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry. 2011; 83: 383-8.
121. Smith MC. Nerve fi bre degeneration in the brain in amyo-trophic lateral sclerosis. J Neurol Neurosurg Psychiatry. 1960; 23: 269-82.
122. Li J, Pan P, Song W, Huang R, Chen K, Shang H. A meta-analysis of diffusion tensor imaging studies in amyotrophic lateral sclerosis. Neurobiol Aging. 2011; 33: 1833-8.
123. Filippini N, Douaud G, Mackay CE, Knight S, Talbot K, Turner MR. Corpus callosum involvement is a consistent feature of amyotrophic lateral sclerosis. Neurology. 2010; 75: 1645-52.
124. Menke RAL, Abraham I, Thiel CS, Filippini N, Knight S, Talbot K, et al. Fractional anisotropy in the posterior limb of the internal capsule and prognosis in amyotrophic lateral sclerosis. Arch Neurol. 2012; 69: 1493-9.
125. van der Graaff MM, Sage CA, Caan MW, Akkerman EM, Lavini C, Majoie CB, et al. Upper and extramotor neuron involvement in early motor neuron disease: a diffusion tensor imaging study. Brain. 2011; 134: 1211-28.
126. Foerster BR, Dwamena BA, Petrou M, Carlos RC, Callaghan BC, Pomper MG. Diagnostic Accuracy Using Diffusion Tensor Imaging in the Diagnosis of ALS: A Meta-analysis. Acad Radiol. 2012; 19: 1075-86.
127. Douaud G, Filippini N, Knight S, Talbot K, Turner MR. Integration of structural and functional magnetic resonance imaging in amyotrophic lateral sclerosis. Brain. 2011; 134: 3470-9.
128. Foerster BR, Callaghan BC, Petrou M, Edden RA, Chenevert TL, Feldman EL. Decreased motor cortex gamma-aminobutyric acid in amyotrophic lateral sclerosis. Neurology. 2012; 78: 1596-600.
129. Carew JD, Nair G, Andersen PM, Wuu J, Gronka S, Hu X, et al. Presymptomatic spinal cord neurometabolic fi ndings in SOD1-positive people at risk for familial ALS. Neurology. 2011; 77: 1370-5.
130. Polymenidou M, Cleveland DW. The seeds of neurode-generation: prion-like spreading in ALS. Cell. 2011; 147: 498-508.
131. Douglass CP, Kandler RH, Shaw PJ, McDermott CJ. An evaluation of neurophysiological criteria used in the diagnosis of motor neuron disease. J Neurol Neurosurg Psychiatry. 2010; 81: 646-9.
132. Haverkamp LJ, Appel V, Appel SH. Natural history of amyotrophic lateral sclerosis in a database population. Validation of a scoring system and a model for survival prediction. Brain. 1995; 118 (Pt 3): 707-19.
133. Turner MR, Bakker M, Sham P et al. Prognostic modelling of therapeutic interventions in amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord. 2002; 3: 15-21.
134. Cedarbaum JM, Stambler N, Malta E et al. The ALS-FRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. BDNF ALS Study Group (Phase III). J.Neurol.Sci. 1999; 169: 13-21.
135. Johnson BS, McCaffery JM, Lindquist S, Gitler AD. A yeast TDP-43 proteinopathy model: Exploring the molecular determinants of TDP-43 aggregation and cellular toxic-ity. Proc Natl Acad Sci U S A. 2008; 105: 6439-44.
136. Bastow EL, Gourlay CW, Tuite MF. Using yeast models to probe the molecular basis of amyotrophic lateral sclerosis. Biochem Soc Trans. 2011; 39: 1482-87.
137. Couthouis J, Hart MP, Shorter J et al. A yeast functional screen predicts new candidate ALS disease genes. Proc Natl Acad Sci U S A. 2011; 108: 20881-90.
138. Oeda T, Shimohama S, Kitagawa N et al. Oxidative stress causes abnormal accumulation of familial amyotrophic lateral sclerosis-related mutant SOD1 in transgenic Caenorhabditis elegans. Hum Mol Genet. 2001; 10: 2013-23.
139. Vaccaro A, Tauffenberger A, Aggad D et al. Mutant TDP-43 and FUS cause age-dependent paralysis and neurodegen-eration in C. elegans. PLoS One. 2012; 7: e31321.
140. Lanson NA, Jr., Maltare A, King H et al. A Drosophila model of FUS-related neurodegeneration reveals genetic interaction between FUS and TDP-43. Hum Mol Genet. 2011; 20: 2510-23.
141. Wang JW, Brent JR, Tomlinson A et al. The ALS-associated proteins FUS and TDP-43 function together to affect Dro-sophila locomotion and life span. J Clin Invest. 2011; 121: 4118-26.
142. Xia R, Liu Y, Yang L et al. Motor neuron apoptosis and neuromuscular junction perturbation are prominent features in a Drosophila model of Fus-mediated ALS. Mol Neurodegener. 2012; 7: 10.
143. Miguel L, Avequin T, Delarue M et al. Accumulation of insoluble forms of FUS protein correlates with toxicity in Drosophila. Neurobiol Aging. 2012; 33: 1008 e1001-1015.
144. Bosco DA, Lemay N, Ko HK et al. Mutant FUS proteins that cause amyotrophic lateral sclerosis incorporate into stress granules. Hum Mol Genet. 2010; 19: 4160-75.
145. Kabashi E, Bercier V, Lissouba A et al. FUS and TARDBP but not SOD1 interact in genetic models of amyotrophic l ateral sclerosis. PLoS Genet. 2011; 7: e1002214.
146. Turner BJ, Talbot K. Transgenics, toxicity and therapeutics in rodent models of mutant SOD1-mediated familial ALS. Prog Neurobiol. 2008; 85: 94-134.
147. Awano T, Johnson GS, Wade CM et al. Genome-wide association analysis reveals a SOD1 mutation in canine degenerative myelopathy that resembles amyotrophic lateral sclerosis. Proc Natl Acad Sci U S A. 2009; 106: 2794-99.
148. Uchida A, Sasaguri H, Kimura N et al. Non-human primate model of amyotrophic lateral sclerosis with cytoplas-mic mislocalization of TDP-43. Brain. 2012; 135: 833-46.