Emerging molecular biomarker targets for amyotrophic lateral sclerosis

Clinica Chimica Acta

Volumn 455, Issue , 2016, Pages 7-14

  Costa, Júlia ^a   de Carvalho, Mamede ^b,c  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^b INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

^c HOSPITAL DE SANTA MARIA   (Portugal)

Author keywords

Amyotrophic lateral sclerosis; Biomarker; Neurofilaments; Progression; Survival

Indexed keywords

BIOLOGICAL MARKER; CELL PROTEIN; COPPER ZINC SUPEROXIDE DISMUTASE; MOLECULAR MARKER; PROTEIN C9ORF72; TAR DNA BINDING PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN;

AMYOTROPHIC LATERAL SCLEROSIS; BRAIN ELECTROPHYSIOLOGY; CEREBROSPINAL FLUID LEVEL; CYTOSKELETON; DIFFUSION WEIGHTED IMAGING; ELECTROMYOGRAPHY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GLYCOBIOLOGY; HUMAN; LOWER MOTOR NEURON; METABOLOMICS; MOLECULAR GENETICS; MOTONEURON; MUTATIONAL ANALYSIS; NERVOUS SYSTEM INFLAMMATION; NEUROFILAMENT; NEUROIMAGING; OXIDATIVE STRESS; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; PROGNOSIS; PROTEIN AGGREGATION; PROTEOMICS; REVIEW; SENSITIVITY AND SPECIFICITY; UPPER MOTOR NEURON; VOLUMETRY; ADULT; CHILD; GENETICS; METABOLISM;

ADULT; AMYOTROPHIC LATERAL SCLEROSIS; BIOMARKERS; CHILD; HUMANS;

EID: 84955315960     PISSN: 00098981     EISSN: 18733492     Source Type: Journal    
DOI: 10.1016/j.cca.2016.01.011     Document Type: Review

References (124)

1. Chio A., Mora G., Calvo A., Mazzini L., Bottacchi E., Mutani R. Parals, epidemiology of ALS in Italy: a 10-year prospective population-based study. Neurology 2009, 72:725-731.
2. Mandrioli J., Faglioni P., Merelli E., Sola P. The epidemiology of ALS in Modena, Italy. Neurology 2003, 60:683-689.
3. Stambler N., Charatan M., Cedarbaum J.M. Prognostic indicators of survival in ALS. ALS CNTF treatment study group. Neurology 1998, 50:66-72.
4. de Carvalho M., Matias T., Coelho F., Evangelista T., Pinto A., Luis M.L. Motor neuron disease presenting with respiratory failure. J. Neurol. Sci. 1996, 139(Suppl):117-122.
5. Gouveia L.O., de Carvalho M. Young-onset sporadic amyotrophic lateral sclerosis: a distinct nosological entity?. Amyotroph. Lateral Scler. 2007, 8:323-327.
6. Costa J., Gomes C., de Carvalho M. Diagnosis, pathogenesis and therapeutic targets in amyotrophic lateral sclerosis. CNS Neurol. Disord. Drug Targets 2010, 9:764-778.
7. Andersen P.M., Abrahams S., Borasio G.D., de Carvalho M., Chio A., Van Damme P., Hardiman O., Kollewe K., Morrison K.E., Petri S., Pradat P.F., Silani V., Tomik B., Wasner M., Weber M. EFNS guidelines on the clinical management of amyotrophic lateral sclerosis (MALS)-revised report of an EFNS task force. Eur. J. Neurol. 2012, 19:360-375.
8. Costa J., Rocha M.L., Ferreira J., Evangelista T., Coelho M., de Carvalho M. Botulinum toxin type-B improves sialorrhea and quality of life in bulbaronset amyotrophic lateral sclerosis. J. Neurol. 2008, 255:545-550.
9. Londral A., Pinto A., Pinto S., Azevedo L., De Carvalho M. Quality of life in amyotrophic lateral sclerosis patients and caregivers: impact of assistive communication from early stages. Muscle Nerve 2015.
10. Turner M.R., Kiernan M.C., Leigh P.N., Talbot K. Biomarkers in amyotrophic lateral sclerosis. Lancet Neurol. 2009, 8:94-109.
11. Tarasiuk J., Kulakowska A., Drozdowski W., Kornhuber J., Lewczuk P. CSF markers in amyotrophic lateral sclerosis. J. Neural Transm. 2012, 119:747-757.
12. Otto M., Bowser R., Turner M., Berry J., Brettschneider J., Connor J., Costa J., Cudkowicz M., Glass J., Jahn O., Lehnert S., Malaspina A., Parnetti L., Petzold A., Shaw P., Sherman A., Steinacker P., Sussmuth S., Teunissen C., Tumani H., Wuolikainen A., Ludolph A., Volcano G. Roadmap and standard operating procedures for biobanking and discovery of neurochemical markers in ALS. Amyotroph. Lateral Scler. 2012, 13:1-10.
13. Turner M.R., Bowser R., Bruijn L., Dupuis L., Ludolph A., McGrath M., Manfredi G., Maragakis N., Miller R.G., Pullman S.L., Rutkove S.B., Shaw P.J., Shefner J., Fischbeck K.H. Mechanisms, models and biomarkers in amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. Frontotemporal Degener 2013, 14(Suppl. 1):19-32.
14. Turner M.R., Hardiman O., Benatar M., Brooks B.R., Chio A., de Carvalho M., Ince P.G., Lin C., Miller R.G., Mitsumoto H., Nicholson G., Ravits J., Shaw P.J., Swash M., Talbot K., Traynor B.J., Van den Berg L.H., Veldink J.H., Vucic S., Kiernan M.C. Controversies and priorities in amyotrophic lateral sclerosis. Lancet Neurol. 2013, 12:310-322.
15. Kruger T., Lautenschlager J., Grosskreutz J., Rhode H. Proteome analysis of body fluids for amyotrophic lateral sclerosis biomarker discovery. Proteomics Clin. Appl. 2013, 7:123-135.
16. Robelin L., Gonzalez De Aguilar J.L. Blood biomarkers for amyotrophic lateral sclerosis: myth or reality?. Biomed. Res. Int. 2014, 2014:525097.
17. Abdelhak A., Junker A., Brettschneider J., Kassubek J., Ludolph A.C., Otto M., Tumani H. Brain-specific cytoskeletal damage markers in cerebrospinal fluid: is there a common pattern between amyotrophic lateral sclerosis and primary progressive multiple sclerosis?. Int. J. Mol. Sci. 2015, 16:17565-17588.
18. de Carvalho M., Dengler R., Eisen A., England J.D., Kaji R., Kimura J., Mills K., Mitsumoto H., Nodera H., Shefner J., Swash M. Electrodiagnostic criteria for diagnosis of ALS. Clin. Neurophysiol. 2008, 119:497-503.
19. Vucic S., Howells J., Trevillion L., Kiernan M.C. Assessment of cortical excitability using threshold tracking techniques. Muscle Nerve 2006, 33:477-486.
20. Bede P., Hardiman O. Lessons of ALS imaging: pitfalls and future directions - a critical review. Neuroimage Clin. 2014, 4:436-443.
21. Leblond C.S., Kaneb H.M., Dion P.A., Rouleau G.A. Dissection of genetic factors associated with amyotrophic lateral sclerosis. Exp. Neurol. 2014, 262(Pt B):91-101.
22. Chio A., Traynor B.J. Motor neuron disease in 2014. Biomarkers for ALS-in search of the promised land. Nat. Rev. Neurol. 2015, 11:72-74.
23. Rosen D.R., Siddique T., Patterson D., Figlewicz D.A., Sapp P., Hentati A., Donaldson D., Goto J., O'Regan J.P., Deng H.X., et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993, 362:59-62.
24. Munch C., Bertolotti A. Exposure of hydrophobic surfaces initiates aggregation of diverse ALS-causing superoxide dismutase-1 mutants. J. Mol. Biol. 2010, 399:512-525.
25. Lee E.B., Lee V.M., Trojanowski J.Q. Gains or losses: molecular mechanisms of TDP43-mediated neurodegeneration. Nat. Rev. Neurosci. 2012, 13:38-50.
26. Rohrer J.D., Isaacs A.M., Mizielinska S., Mead S., Lashley T., Wray S., Sidle K., Fratta P., Orrell R.W., Hardy J., Holton J., Revesz T., Rossor M.N., Warren J.D. C9orf72 expansions in frontotemporal dementia and amyotrophic lateral sclerosis. Lancet Neurol. 2015, 14:291-301.
27. Smith B.N., Newhouse S., Shatunov A., Vance C., Topp S., Johnson L., Miller J., Lee Y., Troakes C., Scott K.M., Jones A., Gray I., Wright J., Hortobagyi T., Al-Sarraj S., Rogelj B., Powell J., Lupton M., Lovestone S., Sapp P.C., Weber M., Nestor P.J., Schelhaas H.J., Asbroek A.A., Silani V., Gellera C., Taroni F., Ticozzi N., Van den Berg L., Veldink J., Van Damme P., Robberecht W., Shaw P.J., Kirby J., Pall H., Morrison K.E., Morris A., de Belleroche J., Vianney de Jong J.M., Baas F., Andersen P.M., Landers J., Brown R.H., Weale M.E., Al-Chalabi A., Shaw C.E. The C9ORF72 expansion mutation is a common cause of ALS+/-FTD in Europe and has a single founder. Eur. J. Hum. Genet. 2013, 21:102-108.
28. Zhang K., Donnelly C.J., Haeusler A.R., Grima J.C., Machamer J.B., Steinwald P., Daley E.L., Miller S.J., Cunningham K.M., Vidensky S., Gupta S., Thomas M.A., Hong I., Chiu S.L., Huganir R.L., Ostrow L.W., Matunis M.J., Wang J., Sattler R., Lloyd T.E., Rothstein J.D. The C9orf72 repeat expansion disrupts nucleocytoplasmic transport. Nature 2015, 525:56-61.
29. Freibaum B.D., Lu Y., Lopez-Gonzalez R., Kim N.C., Almeida S., Lee K.H., Badders N., Valentine M., Miller B.L., Wong P.C., Petrucelli L., Kim H.J., Gao F.B., Taylor J.P. GGGGCC repeat expansion in C9orf72 compromises nucleocytoplasmic transport. Nature 2015, 525:129-133.
30. Yuan A., Rao M.V., Veeranna, Nixon R.A. Neurofilaments at a glance. J. Cell Sci. 2012, 125:3257-3263.
31. Munoz D.G., Greene C., Perl D.P., Selkoe D.J. Accumulation of phosphorylated neurofilaments in anterior horn motoneurons of amyotrophic lateral sclerosis patients. J. Neuropathol. Exp. Neurol. 1988, 47:9-18.
32. Laser-Azogui A., Kornreich M., Malka-Gibor E., Beck R. Neurofilament assembly and function during neuronal development. Curr. Opin. Cell Biol. 2015, 32:92-101.
33. Yuzwa S.A., Shan X., Macauley M.S., Clark T., Skorobogatko Y., Vosseller K., Vocadlo D.J. Increasing O-GlcNAc slows neurodegeneration and stabilizes tau against aggregation. Nat. Chem. Biol. 2012, 8:393-399.
34. Shan X., Vocadlo D.J., Krieger C. Reduced protein O-glycosylation in the nervous system of the mutant SOD1 transgenic mouse model of amyotrophic lateral sclerosis. Neurosci. Lett. 2012, 516:296-301.
35. Brettschneider J., Petzold A., Sussmuth S.D., Ludolph A.C., Tumani H. Axonal damage markers in cerebrospinal fluid are increased in ALS. Neurology 2006, 66:852-856.
36. Reijn T.S., Abdo W.F., Schelhaas H.J., Verbeek M.M. CSF neurofilament protein analysis in the differential diagnosis of ALS. J. Neurol. 2009, 256:615-619.
37. Ganesalingam J., An J., Shaw C.E., Shaw G., Lacomis D., Bowser R. Combination of neurofilament heavy chain and complement C3 as CSF biomarkers for ALS. J. Neurochem. 2011, 117:528-537.
38. Ganesalingam J., An J., Bowser R., Andersen P.M., Shaw C.E. pNfH is a promising biomarker for ALS. Amyotroph. Lateral Scler. Frontotemporal Degener 2013, 14:146-149.
39. Boylan K.B., Glass J.D., Crook J.E., Yang C., Thomas C.S., Desaro P., Johnston A., Overstreet K., Kelly C., Polak M., Shaw G. Phosphorylated neurofilament heavy subunit (pNF-H) in peripheral blood and CSF as a potential prognostic biomarker in amyotrophic lateral sclerosis. J. Neurol. Neurosurg. Psychiatry 2013, 84:467-472.
40. Lu C.H., Petzold A., Topping J., Allen K., Macdonald-Wallis C., Clarke J., Pearce N., Kuhle J., Giovannoni G., Fratta P., Sidle K., Fish M., Orrell R., Howard R., Greensmith L., Malaspina A. Plasma neurofilament heavy chain levels and disease progression in amyotrophic lateral sclerosis: insights from a longitudinal study. J. Neurol. Neurosurg. Psychiatry 2015, 86:565-573.
41. Lehnert S., Costa J., de Carvalho M., Kirby J., Kuzma-Kozakiewicz M., Morelli C., Robberecht W., Shaw P., Silani V., Steinacker P., Tumani H., Van Damme P., Ludolph A., Otto M. Multicentre quality control evaluation of different biomarker candidates for amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. Frontotemporal Degener 2014, 15:344-350.
42. Steinacker P., Feneberg E., Weishaupt J., Brettschneider J., Tumani H., Andersen P.M., von Arnim C.A., Bohm S., Kassubek J., Kubisch C., Lule D., Muller H.P., Muche R., Pinkhardt E., Oeckl P., Rosenbohm A., Anderl-Straub S., Volk A.E., Weydt P., Ludolph A.C., Otto M. Neurofilaments in the diagnosis of motoneuron diseases: a prospective study on 455 patients. J. Neurol. Neurosurg. Psychiatry 2015.
43. Goncalves M., Tillack L., de Carvalho M., Pinto S., Conradt H.S., Costa J. Phosphoneurofilament heavy chain and N-glycomics from the cerebrospinal fluid in amyotrophic lateral sclerosis. Clin. Chim. Acta 2015, 438:342-349.
44. Sellner J., Davies N.W., Howard R.S., Petzold A. Neurofilament heavy chain as a marker of neuroaxonal pathology and prognosis in acute encephalitis. Eur. J. Neurol. 2014, 21:845-850.
45. Gresle M.M., Liu Y., Dagley L.F., Haartsen J., Pearson F., Purcell A.W., Laverick L., Petzold A., Lucas R.M., Van der Walt A., Prime H., Morris D.R., Taylor B.V., Ausimmune C., Shaw G., Butzkueven H. Serum phosphorylated neurofilament-heavy chain levels in multiple sclerosis patients. J. Neurol. Neurosurg. Psychiatry 2014, 85:1209-1213.
46. Rosengren L.E., Karlsson J.E., Karlsson J.O., Persson L.I., Wikkelso C. Patients with amyotrophic lateral sclerosis and other neurodegenerative diseases have increased levels of neurofilament protein in CSF. J. Neurochem. 1996, 67:2013-2018.
47. Norgren N., Rosengren L., Stigbrand T. Elevated neurofilament levels in neurological diseases. Brain Res. 2003, 987:25-31.
48. Zetterberg H., Jacobsson J., Rosengren L., Blennow K., Andersen P.M. Cerebrospinal fluid neurofilament light levels in amyotrophic lateral sclerosis: impact of SOD1 genotype. Eur. J. Neurol. 2007, 14:1329-1333.
49. Tortelli R., Ruggieri M., Cortese R., D'Errico E., Capozzo R., Leo A., Mastrapasqua M., Zoccolella S., Leante R., Livrea P., Logroscino G., Simone I.L. Elevated cerebrospinal fluid neurofilament light levels in patients with amyotrophic lateral sclerosis: a possible marker of disease severity and progression. Eur. J. Neurol. 2012, 19:1561-1567.
50. Gaiottino J., Norgren N., Dobson R., Topping J., Nissim A., Malaspina A., Bestwick J.P., Monsch A.U., Regeniter A., Lindberg R.L., Kappos L., Leppert D., Petzold A., Giovannoni G., Kuhle J. Increased neurofilament light chain blood levels in neurodegenerative neurological diseases. PLoS One 2013, 8.
51. Lu C.H., Macdonald-Wallis C., Gray E., Pearce N., Petzold A., Norgren N., Giovannoni G., Fratta P., Sidle K., Fish M., Orrell R., Howard R., Talbot K., Greensmith L., Kuhle J., Turner M.R., Malaspina A. Neurofilament light chain: a prognostic biomarker in amyotrophic lateral sclerosis. Neurology 2015, 84:2247-2257.
52. Puentes F., Topping J., Kuhle J., van der Star B.J., Douiri A., Giovannoni G., Baker D., Amor S., Malaspina A. Immune reactivity to neurofilament proteins in the clinical staging of amyotrophic lateral sclerosis. J. Neurol. Neurosurg. Psychiatry 2014, 85:274-278.
53. Menke R.A., Gray E., Lu C.H., Kuhle J., Talbot K., Malaspina A., Turner M.R. CSF neurofilament light chain reflects corticospinal tract degeneration in ALS. Ann. Clin. Transl. Neurol. 2015, 2:748-755.
54. R. Tortelli, M. Copetti, M. Ruggieri, R. Cortese, R. Capozzo, A. Leo, E. D'Errico, M. Mastrapasqua, S. Zoccolella, F. Pellegrini, I.L. Simone, G. Logroscino, Cerebrospinal fluid neurofilament light chain levels: marker of progression to generalized amyotrophic lateral sclerosis, Eur. J. Neurol. 22 (2015) 215-218.
55. Simpson E.P., Henry Y.K., Henkel J.S., Smith R.G., Appel S.H. Increased lipid peroxidation in sera of ALS patients: a potential biomarker of disease burden. Neurology 2004, 62:1758-1765.
56. Tohgi H., Abe T., Yamazaki K., Murata T., Ishizaki E., Isobe C. Remarkable increase in cerebrospinal fluid 3-nitrotyrosine in patients with sporadic amyotrophic lateral sclerosis. Ann. Neurol. 1999, 46:129-131.
57. Kokic A.N., Stevic Z., Stojanovic S., Blagojevic D.P., Jones D.R., Pavlovic S., Niketic V., Apostolski S., Spasic M.B. Biotransformation of nitric oxide in the cerebrospinal fluid of amyotrophic lateral sclerosis patients. Redox Rep. 2005, 10:265-270.
58. Boll M.C., Alcaraz-Zubeldia M., Montes S., Murillo-Bonilla L., Rios C. Raised nitrate concentration and low SOD activity in the CSF of sporadic ALS patients. Neurochem. Res. 2003, 28:699-703.
59. Ihara Y., Nobukuni K., Takata H., Hayabara T. Oxidative stress and metal content in blood and cerebrospinal fluid of amyotrophic lateral sclerosis patients with and without a Cu, Zn-superoxide dismutase mutation. Neurol. Res. 2005, 27:105-108.
60. Frutiger K., Lukas T.J., Gorrie G., Ajroud-Driss S., Siddique T. Gender difference in levels of Cu/Zn superoxide dismutase (SOD1) in cerebrospinal fluid of patients with amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. 2008, 9:184-187.
61. Zetterstrom P., Andersen P.M., Brannstrom T., Marklund S.L. Misfolded superoxide dismutase-1 in CSF from amyotrophic lateral sclerosis patients. J. Neurochem. 2011, 117:91-99.
62. Kasai T., Tokuda T., Ishigami N., Sasayama H., Foulds P., Mitchell D.J., Mann D.M., Allsop D., Nakagawa M. Increased TDP-43 protein in cerebrospinal fluid of patients with amyotrophic lateral sclerosis. Acta Neuropathol. 2009, 117:55-62.
63. Noto Y., Shibuya K., Sato Y., Kanai K., Misawa S., Sawai S., Mori M., Uchiyama T., Isose S., Nasu S., Sekiguchi Y., Fujimaki Y., Kasai T., Tokuda T., Nakagawa M., Kuwabara S. Elevated CSF TDP-43 levels in amyotrophic lateral sclerosis: specificity, sensitivity, and a possible prognostic value. Amyotroph. Lateral Scler. 2011, 12:140-143.
64. Hosokawa M., Arai T., Yamashita M., Tsuji H., Nonaka T., Masuda-Suzukake M., Tamaoka A., Hasegawa M., Akiyama H. Differential diagnosis of amyotrophic lateral sclerosis from Guillain-Barre syndrome by quantitative determination of TDP-43 in cerebrospinal fluid. Int. J. Neurosci. 2014, 124:344-349.
65. Feneberg E., Steinacker P., Lehnert S., Schneider A., Walther P., Thal D.R., Linsenmeier M., Ludolph A.C., Otto M. Limited role of free TDP-43 as a diagnostic tool in neurodegenerative diseases. Amyotroph. Lateral Scler. Frontotemporal Degener 2014, 15:351-356.
66. Gomes C., Keller S., Altevogt P., Costa J. Evidence for secretion of Cu, Zn superoxide dismutase via exosomes from a cell model of amyotrophic lateral sclerosis. Neurosci. Lett. 2007, 428:43-46.
67. Grad L.I., Yerbury J.J., Turner B.J., Guest W.C., Pokrishevsky E., O'Neill M.A., Yanai A., Silverman J.M., Zeineddine R., Corcoran L., Kumita J.R., Luheshi L.M., Yousefi M., Coleman B.M., Hill A.F., Plotkin S.S., Mackenzie I.R., Cashman N.R. Intercellular propagated misfolding of wild-type Cu/Zn superoxide dismutase occurs via exosome-dependent and -independent mechanisms. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:3620-3625.
68. Asai H., Ikezu S., Tsunoda S., Medalla M., Luebke J., Haydar T., Wolozin B., Butovsky O., Kugler S., Ikezu T. Depletion of microglia and inhibition of exosome synthesis halt tau propagation. Nat. Neurosci. 2015, 18:1584-1593.
69. Chiasserini D., van Weering J.R., Piersma S.R., Pham T.V., Malekzadeh A., Teunissen C.E., de Wit H., Jimenez C.R. Proteomic analysis of cerebrospinal fluid extracellular vesicles: a comprehensive dataset. J. Proteome 2014, 106:191-204.
70. Su Z., Zhang Y., Gendron T.F., Bauer P.O., Chew J., Yang W.Y., Fostvedt E., Jansen-West K., Belzil V.V., Desaro P., Johnston A., Overstreet K., Oh S.Y., Todd P.K., Berry J.D., Cudkowicz M.E., Boeve B.F., Dickson D., Floeter M.K., Traynor B.J., Morelli C., Ratti A., Silani V., Rademakers R., Brown R.H., Rothstein J.D., Boylan K.B., Petrucelli L., Disney M.D. Discovery of a biomarker and lead small molecules to target r(GGGGCC)-associated defects in c9FTD/ALS. Neuron 2014, 83:1043-1050.
71. Grossman M., Elman L., McCluskey L., McMillan C.T., Boller A., Powers J., Rascovsky K., Hu W., Shaw L., Irwin D.J., Lee V.M., Trojanowski J.Q. Phosphorylated tau as a candidate biomarker for amyotrophic lateral sclerosis. JAMA Neurol. 2014, 71:442-448.
72. Wilke C., Deuschle C., Rattay T.W., Maetzler W., Synofzik M. Total tau is increased, but phosphorylated tau not decreased, in cerebrospinal fluid in amyotrophic lateral sclerosis. Neurobiol. Aging 2015, 36:1072-1074.
73. Pronto-Laborinho A.C., Pinto S., de Carvalho M. Roles of vascular endothelial growth factor in amyotrophic lateral sclerosis. Biomed. Res. Int. 2014, 2014:947513.
74. Devos D., Moreau C., Lassalle P., Perez T., De Seze J., Brunaud-Danel V., Destee A., Tonnel A.B., Just N. Low levels of the vascular endothelial growth factor in CSF from early ALS patients. Neurology 2004, 62:2127-2129.
75. Just N., Moreau C., Lassalle P., Gosset P., Perez T., Brunaud-Danel V., Wallaert B., Destee A., Defebvre L., Tonnel A.B., Devos D. High erythropoietin and low vascular endothelial growth factor levels in cerebrospinal fluid from hypoxemic ALS patients suggest an abnormal response to hypoxia. Neuromuscul. Disord. 2007, 17:169-173.
76. Carilho R., de Carvalho M., Kuehl U., Pinto S., Pinto A., Kromminga A., Costa J. Erythropoietin and amyotrophic lateral sclerosis: plasma level determination. Amyotroph. Lateral Scler. 2011, 12:439-443.
77. Carilho R., de Carvalho M., Swash M., Pinto S., Pinto A., Costa J. Vascular endothelial growth factor and amyotrophic lateral sclerosis: the interplay with exercise and noninvasive ventilation. Muscle Nerve 2014, 49:545-550.
78. Shepheard S.R., Chataway T., Schultz D.W., Rush R.A., Rogers M.L. The extracellular domain of neurotrophin receptor p75 as a candidate biomarker for amyotrophic lateral sclerosis. PLoS One 2014, 9.
79. Moreau C., Devos D., Brunaud-Danel V., Defebvre L., Perez T., Destee A., Tonnel A.B., Lassalle P., Just N. Elevated IL-6 and TNF-alpha levels in patients with ALS: inflammation or hypoxia?. Neurology 2005, 65:1958-1960.
80. Zhou J.Y., Afjehi-Sadat L., Asress S., Duong D.M., Cudkowicz M., Glass J.D., Peng J. Galectin-3 is a candidate biomarker for amyotrophic lateral sclerosis: discovery by a proteomics approach. J. Proteome Res. 2010, 9:5133-5141.
81. Varghese A.M., Sharma A., Mishra P., Vijayalakshmi K., Harsha H.C., Sathyaprabha T.N., Bharath S.M., Nalini A., Alladi P.A., Raju T.R. Chitotriosidase - a putative biomarker for sporadic amyotrophic lateral sclerosis. Clin. Proteomics 2013, 10:19.
82. Davoli A., Greco V., Spalloni A., Guatteo E., Neri C., Rizzo G.R., Cordella A., Romigi A., Cortese C., Bernardini S., Sarchielli P., Cardaioli G., Calabresi P., Mercuri N.B., Urbani A., Longone P. Evidence of hydrogen sulfide involvement in amyotrophic lateral sclerosis. Ann. Neurol. 2015, 77:697-709.
83. Freischmidt A., Muller K., Zondler L., Weydt P., Mayer B., von Arnim C.A., Hubers A., Dorst J., Otto M., Holzmann K., Ludolph A.C., Danzer K.M., Weishaupt J.H. Serum microRNAs in sporadic amyotrophic lateral sclerosis. Neurobiol. Aging 2015, 36. (2660 e2615-2620).
84. Toivonen J.M., Manzano R., Olivan S., Zaragoza P., Garcia-Redondo A., Osta R. MicroRNA-206: a potential circulating biomarker candidate for amyotrophic lateral sclerosis. PLoS One 2014, 9.
85. Pasinetti G.M., Ungar L.H., Lange D.J., Yemul S., Deng H., Yuan X., Brown R.H., Cudkowicz M.E., Newhall K., Peskind E., Marcus S., Ho L. Identification of potential CSF biomarkers in ALS. Neurology 2006, 66:1218-1222.
86. Brettschneider J., Lehmensiek V., Mogel H., Pfeifle M., Dorst J., Hendrich C., Ludolph A.C., Tumani H. Proteome analysis reveals candidate markers of disease progression in amyotrophic lateral sclerosis (ALS). Neurosci. Lett. 2010, 468:23-27.
87. von Neuhoff N., Oumeraci T., Wolf T., Kollewe K., Bewerunge P., Neumann B., Brors B., Bufler J., Wurster U., Schlegelberger B., Dengler R., Zapatka M., Petri S. Monitoring CSF proteome alterations in amyotrophic lateral sclerosis: obstacles and perspectives in translating a novel marker panel to the clinic. PLoS One 2012, 7.
88. Su X.W., Simmons Z., Mitchell R.M., Kong L., Stephens H.E., Connor J.R. Biomarker-based predictive models for prognosis in amyotrophic lateral sclerosis. JAMA Neurol. 2013, 70:1505-1511.
89. Edri-Brami M., Rosental B., Hayoun D., Welt M., Rosen H., Wirguin I., Nefussy B., Drory V.E., Porgador A., Lichtenstein R.G. Glycans in sera of amyotrophic lateral sclerosis patients and their role in killing neuronal cells. PLoS One 2012, 7.
90. Wuolikainen A., Andersen P.M., Moritz T., Marklund S.L., Antti H. ALS patients with mutations in the SOD1 gene have an unique metabolomic profile in the cerebrospinal fluid compared with ALS patients without mutations. Mol. Genet. Metab. 2012, 105:472-478.
91. Lawton K.A., Cudkowicz M.E., Brown M.V., Alexander D., Caffrey R., Wulff J.E., Bowser R., Lawson R., Jaffa M., Milburn M.V., Ryals J.A., Berry J.D. Biochemical alterations associated with ALS. Amyotroph. Lateral Scler. 2012, 13:110-118.
92. Lawton K.A., Brown M.V., Alexander D., Li Z., Wulff J.E., Lawson R., Jaffa M., Milburn M.V., Ryals J.A., Bowser R., Cudkowicz M.E., Berry J.D., Northeast A.L.S.C. Plasma metabolomic biomarker panel to distinguish patients with amyotrophic lateral sclerosis from disease mimics. Amyotroph. Lateral Scler. Frontotemporal Degener 2014, 15:362-370.
93. Abraham A., Drory V.E. Influence of serum uric acid levels on prognosis and survival in amyotrophic lateral sclerosis: a meta-analysis. J. Neurol. 2014, 261:1133-1138.
94. Blasco H., Corcia P., Pradat P.F., Bocca C., Gordon P.H., Veyrat-Durebex C., Mavel S., Nadal-Desbarats L., Moreau C., Devos D., Andres C.R., Emond P. Metabolomics in cerebrospinal fluid of patients with amyotrophic lateral sclerosis: an untargeted approach via high-resolution mass spectrometry. J. Proteome Res. 2013, 12:3746-3754.
95. Gray E., Larkin J.R., Claridge T.D., Talbot K., Sibson N.R., Turner M.R. The longitudinal cerebrospinal fluid metabolomic profile of amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. Frontotemporal Degener 2015, 16:456-463.
96. Beghi E., Balzarini C., Bogliun G., Logroscino G., Manfredi L., Mazzini L., Micheli A., Millul A., Poloni M., Riva R., Salmoiraghi F., Tonini C., Vitelli E., A.L.S.S.G.Italian Reliability of the El Escorial diagnostic criteria for amyotrophic lateral sclerosis. Neuroepidemiology 2002, 21:265-270.
97. Nzwalo H., de Abreu D., Swash M., Pinto S., de Carvalho M. Delayed diagnosis in ALS: the problem continues. J. Neurol. Sci. 2014, 343:173-175.
98. Hadano S., Hand C.K., Osuga H., Yanagisawa Y., Otomo A., Devon R.S., Miyamoto N., Showguchi-Miyata J., Okada Y., Singaraja R., Figlewicz D.A., Kwiatkowski T., Hosler B.A., Sagie T., Skaug J., Nasir J., Brown R.H., Scherer S.W., Rouleau G.A., Hayden M.R., Ikeda J.E. A gene encoding a putative GTPase regulator is mutated in familial amyotrophic lateral sclerosis 2. Nat. Genet. 2001, 29:166-173.
99. Hadano S., Benn S.C., Kakuta S., Otomo A., Sudo K., Kunita R., Suzuki-Utsunomiya K., Mizumura H., Shefner J.M., Cox G.A., Iwakura Y., Brown R.H., Ikeda J.E. Mice deficient in the Rab5 guanine nucleotide exchange factor ALS2/alsin exhibit age-dependent neurological deficits and altered endosome trafficking. Hum. Mol. Genet. 2006, 15:233-250.
100. Hand C.K., Khoris J., Salachas F., Gros-Louis F., Lopes A.A., Mayeux-Portas V., Brewer C.G., Brown R.H., Meininger V., Camu W., Rouleau G.A. A novel locus for familial amyotrophic lateral sclerosis, on chromosome 18q. Am. J. Hum. Genet. 2002, 70:251-256.
101. Chen Y.Z., Bennett C.L., Huynh H.M., Blair I.P., Puls I., Irobi J., Dierick I., Abel A., Kennerson M.L., Rabin B.A., Nicholson G.A., Auer-Grumbach M., Wagner K., De Jonghe P., Griffin J.W., Fischbeck K.H., Timmerman V., Cornblath D.R., Chance P.F. DNA/RNA helicase gene mutations in a form of juvenile amyotrophic lateral sclerosis (ALS4). Am. J. Hum. Genet. 2004, 74:1128-1135.
102. Orlacchio A., Babalini C., Borreca A., Patrono C., Massa R., Basaran S., Munhoz R.P., Rogaeva E.A., St George-Hyslop P.H., Bernardi G., Kawarai T. SPATACSIN mutations cause autosomal recessive juvenile amyotrophic lateral sclerosis. Brain 2010, 133:591-598.
103. Kwiatkowski T.J., Bosco D.A., Leclerc A.L., Tamrazian E., Vanderburg C.R., Russ C., Davis A., Gilchrist J., Kasarskis E.J., Munsat T., Valdmanis P., Rouleau G.A., Hosler B.A., Cortelli P., de Jong P.J., Yoshinaga Y., Haines J.L., Pericak-Vance M.A., Yan J., Ticozzi N., Siddique T., McKenna-Yasek D., Sapp P.C., Horvitz H.R., Landers J.E., Brown R.H. Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 2009, 323:1205-1208.
104. Vance C., Rogelj B., Hortobagyi T., De Vos K.J., Nishimura A.L., Sreedharan J., Hu X., Smith B., Ruddy D., Wright P., Ganesalingam J., Williams K.L., Tripathi V., Al-Saraj S., Al-Chalabi A., Leigh P.N., Blair I.P., Nicholson G., de Belleroche J., Gallo J.M., Miller C.C., Shaw C.E. Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 2009, 323:1208-1211.
105. Sapp P.C., Hosler B.A., McKenna-Yasek D., Chin W., Gann A., Genise H., Gorenstein J., Huang M., Sailer W., Scheffler M., Valesky M., Haines J.L., Pericak-Vance M., Siddique T., Horvitz H.R., Brown R.H. Identification of two novel loci for dominantly inherited familial amyotrophic lateral sclerosis. Am. J. Hum. Genet. 2003, 73:397-403.
106. Nishimura A.L., Mitne-Neto M., Silva H.C., Richieri-Costa A., Middleton S., Cascio D., Kok F., Oliveira J.R., Gillingwater T., Webb J., Skehel P., Zatz M. A mutation in the vesicle-trafficking protein VAPB causes late-onset spinal muscular atrophy and amyotrophic lateral sclerosis. Am. J. Hum. Genet. 2004, 75:822-831.
107. Greenway M.J., Andersen P.M., Russ C., Ennis S., Cashman S., Donaghy C., Patterson V., Swingler R., Kieran D., Prehn J., Morrison K.E., Green A., Acharya K.R., Brown R.H., Hardiman O. ANG mutations segregate with familial and 'sporadic' amyotrophic lateral sclerosis. Nat. Genet. 2006, 38:411-413.
108. Kabashi E., Valdmanis P.N., Dion P., Spiegelman D., McConkey B.J., Vande Velde C., Bouchard J.P., Lacomblez L., Pochigaeva K., Salachas F., Pradat P.F., Camu W., Meininger V., Dupre N., Rouleau G.A. TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat. Genet. 2008, 40:572-574.
109. Sreedharan J., Blair I.P., Tripathi V.B., Hu X., Vance C., Rogelj B., Ackerley S., Durnall J.C., Williams K.L., Buratti E., Baralle F., de Belleroche J., Mitchell J.D., Leigh P.N., Al-Chalabi A., Miller C.C., Nicholson G., Shaw C.E. TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science 2008, 319:1668-1672.
110. Chow C.Y., Landers J.E., Bergren S.K., Sapp P.C., Grant A.E., Jones J.M., Everett L., Lenk G.M., McKenna-Yasek D.M., Weisman L.S., Figlewicz D., Brown R.H., Meisler M.H. Deleterious variants of FIG4, a phosphoinositide phosphatase, in patients with ALS. Am. J. Hum. Genet. 2009, 84:85-88.
111. Maruyama H., Morino H., Ito H., Izumi Y., Kato H., Watanabe Y., Kinoshita Y., Kamada M., Nodera H., Suzuki H., Komure O., Matsuura S., Kobatake K., Morimoto N., Abe K., Suzuki N., Aoki M., Kawata A., Hirai T., Kato T., Ogasawara K., Hirano A., Takumi T., Kusaka H., Hagiwara K., Kaji R., Kawakami H. Mutations of optineurin in amyotrophic lateral sclerosis. Nature 2010, 465:223-226.
112. Elden A.C., Kim H.J., Hart M.P., Chen-Plotkin A.S., Johnson B.S., Fang X., Armakola M., Geser F., Greene R., Lu M.M., Padmanabhan A., Clay-Falcone D., McCluskey L., Elman L., Juhr D., Gruber P.J., Rub U., Auburger G., Trojanowski J.Q., Lee V.M., Van Deerlin V.M., Bonini N.M., Gitler A.D. Ataxin-2 intermediate-length polyglutamine expansions are associated with increased risk for ALS. Nature 2010, 466:1069-1075.
113. Johnson J.O., Mandrioli J., Benatar M., Abramzon Y., Van Deerlin V.M., Trojanowski J.Q., Gibbs J.R., Brunetti M., Gronka S., Wuu J., Ding J., McCluskey L., Martinez-Lage M., Falcone D., Hernandez D.G., Arepalli S., Chong S., Schymick J.C., Rothstein J., Landi F., Wang Y.D., Calvo A., Mora G., Sabatelli M., Monsurro M.R., Battistini S., Salvi F., Spataro R., Sola P., Borghero G., I.Consortium, Galassi G., Scholz S.W., Taylor J.P., Restagno G., Chio A., Traynor B.J. Exome sequencing reveals VCP mutations as a cause of familial ALS. Neuron 2010, 68:857-864.
114. Deng H.X., Chen W., Hong S.T., Boycott K.M., Gorrie G.H., Siddique N., Yang Y., Fecto F., Shi Y., Zhai H., Jiang H., Hirano M., Rampersaud E., Jansen G.H., Donkervoort S., Bigio E.H., Brooks B.R., Ajroud K., Sufit R.L., Haines J.L., Mugnaini E., Pericak-Vance M.A., Siddique T. Mutations in UBQLN2 cause dominant X-linked juvenile and adult-onset ALS and ALS/dementia. Nature 2011, 477:211-215.
115. Al-Saif A., Al-Mohanna F., Bohlega S. A mutation in sigma-1 receptor causes juvenile amyotrophic lateral sclerosis. Ann. Neurol. 2011, 70:913-919.
116. Parkinson N., Ince P.G., Smith M.O., Highley R., Skibinski G., Andersen P.M., Morrison K.E., Pall H.S., Hardiman O., Collinge J., Shaw P.J., Fisher E.M., M.R.C.P.i.A.Study, F.R.Consortium ALS phenotypes with mutations in CHMP2B (charged multivesicular body protein 2B). Neurology 2006, 67:1074-1077.
117. Wu C.H., Fallini C., Ticozzi N., Keagle P.J., Sapp P.C., Piotrowska K., Lowe P., Koppers M., McKenna-Yasek D., Baron D.M., Kost J.E., Gonzalez-Perez P., Fox A.D., Adams J., Taroni F., Tiloca C., Leclerc A.L., Chafe S.C., Mangroo D., Moore M.J., Zitzewitz J.A., Xu Z.S., van den Berg L.H., Glass J.D., Siciliano G., Cirulli E.T., Goldstein D.B., Salachas F., Meininger V., Rossoll W., Ratti A., Gellera C., Bosco D.A., Bassell G.J., Silani V., Drory V.E., Brown R.H., Landers J.E. Mutations in the profilin 1 gene cause familial amyotrophic lateral sclerosis. Nature 2012, 488:499-503.
118. Takahashi Y., Fukuda Y., Yoshimura J., Toyoda A., Kurppa K., Moritoyo H., Belzil V.V., Dion P.A., Higasa K., Doi K., Ishiura H., Mitsui J., Date H., Ahsan B., Matsukawa T., Ichikawa Y., Moritoyo T., Ikoma M., Hashimoto T., Kimura F., Murayama S., Onodera O., Nishizawa M., Yoshida M., Atsuta N., Sobue G., JaCals, Fifita J.A., Williams K.L., Blair I.P., Nicholson G.A., Gonzalez-Perez P., Brown R.H., Nomoto M., Elenius K., Rouleau G.A., Fujiyama A., Morishita S., Goto J., Tsuji S. ERBB4 mutations that disrupt the neuregulin-ErbB4 pathway cause amyotrophic lateral sclerosis type 19. Am. J. Hum. Genet. 2013, 93:900-905.
119. Kim H.J., Kim N.C., Wang Y.D., Scarborough E.A., Moore J., Diaz Z., MacLea K.S., Freibaum B., Li S., Molliex A., Kanagaraj A.P., Carter R., Boylan K.B., Wojtas A.M., Rademakers R., Pinkus J.L., Greenberg S.A., Trojanowski J.Q., Traynor B.J., Smith B.N., Topp S., Gkazi A.S., Miller J., Shaw C.E., Kottlors M., Kirschner J., Pestronk A., Li Y.R., Ford A.F., Gitler A.D., Benatar M., King O.D., Kimonis V.E., Ross E.D., Weihl C.C., Shorter J., Taylor J.P. Mutations in prion-like domains in hnRNPA2B1 and hnRNPA1 cause multisystem proteinopathy and ALS. Nature 2013, 495:467-473.
120. Johnson J.O., Pioro E.P., Boehringer A., Chia R., Feit H., Renton A.E., Pliner H.A., Abramzon Y., Marangi G., Winborn B.J., Gibbs J.R., Nalls M.A., Morgan S., Shoai M., Hardy J., Pittman A., Orrell R.W., Malaspina A., Sidle K.C., Fratta P., Harms M.B., Baloh R.H., Pestronk A., Weihl C.C., Rogaeva E., Zinman L., Drory V.E., Borghero G., Mora G., Calvo A., Rothstein J.D., I.Consortium, Drepper C., Sendtner M., Singleton A.B., Taylor J.P., Cookson M.R., Restagno G., Sabatelli M., Bowser R., Chio A., Traynor B.J. Mutations in the Matrin 3 gene cause familial amyotrophic lateral sclerosis. Nat. Neurosci. 2014, 17:664-666.
121. Smith B.N., Ticozzi N., Fallini C., Gkazi A.S., Topp S., Kenna K.P., Scotter E.L., Kost J., Keagle P., Miller J.W., Calini D., Vance C., Danielson E.W., Troakes C., Tiloca C., Al-Sarraj S., Lewis E.A., King A., Colombrita C., Pensato V., Castellotti B., de Belleroche J., Baas F., ten Asbroek A.L., Sapp P.C., McKenna-Yasek D., McLaughlin R.L., Polak M., Asress S., Esteban-Perez J., Munoz-Blanco J.L., Simpson M., S.Consortium, van Rheenen W., Diekstra F.P., Lauria G., Duga S., Corti S., Cereda C., Corrado L., Soraru G., Morrison K.E., Williams K.L., Nicholson G.A., Blair I.P., Dion P.A., Leblond C.S., Rouleau G.A., Hardiman O., Veldink J.H., Van den Berg L.H., Al-Chalabi A., Pall H., Shaw P.J., Turner M.R., Talbot K., Taroni F., Garcia-Redondo A., Wu Z., Glass J.D., Gellera C., Ratti A., Brown R.H., Silani V., Shaw C.E., Landers J.E. Exome-wide rare variant analysis identifies TUBA4A mutations associated with familial ALS. Neuron 2014, 84:324-331.
122. Hosler B.A., Siddique T., Sapp P.C., Sailor W., Huang M.C., Hossain A., Daube J.R., Nance M., Fan C., Kaplan J., Hung W.Y., McKenna-Yasek D., Haines J.L., Pericak-Vance M.A., Horvitz H.R., Brown R.H. Linkage of familial amyotrophic lateral sclerosis with frontotemporal dementia to chromosome 9q21-q22. JAMA 2000, 284:1664-1669.
123. De Jesus-Hernandez M., Mackenzie I.R., Boeve B.F., Boxer A.L., Baker M., Rutherford N.J., Nicholson A.M., Finch N.A., Flynn H., Adamson J., Kouri N., Wojtas A., Sengdy P., Hsiung G.Y., Karydas A., Seeley W.W., Josephs K.A., Coppola G., Geschwind D.H., Wszolek Z.K., Feldman H., Knopman D.S., Petersen R.C., Miller B.L., Dickson D.W., Boylan K.B., Graff-Radford N.R., Rademakers R. Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 2011, 72:245-256.
124. Bannwarth S., Ait-El-Mkadem S., Chaussenot A., Genin E.C., Lacas-Gervais S., Fragaki K., Berg-Alonso L., Kageyama Y., Serre V., Moore D.G., Verschueren A., Rouzier C., Le Ber I., Auge G., Cochaud C., Lespinasse F., N'Guyen K., de Septenville A., Brice A., Yu-Wai-Man P., Sesaki H., Pouget J., Paquis-Flucklinger V. A mitochondrial origin for frontotemporal dementia and amyotrophic lateral sclerosis through CHCHD10 involvement. Brain 2014, 137:2329-2345.