Heat shock factor 1 over-expression protects against exposure of hydrophobic residues on mutant SOD1 and early mortality in a mouse model of amyotrophic lateral sclerosis

Molecular Neurodegeneration

Volumn 8, Issue 1, 2013, Pages

  Lin, Pei Yi ^a   Simon, Sharotka M ^c   Koh, Won Kyun ^d   Folorunso, Oluwarotimi ^a   Umbaugh, C Samuel ^a,b   Pierce, Anson ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

^c BRANDEIS UNIVERSITY   (United States)

^d UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

Aggregation; Amyotrophic lateral sclerosis; Heat shock factor 1; Protein surface hydrophobicity; Superoxide dismutase

Indexed keywords

CHAPERONE; COPPER; HEAT SHOCK TRANSCRIPTION FACTOR 1;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; BINDING SITE; CONTROLLED STUDY; CYTOSKELETON; ENERGY METABOLISM; FEMALE; HEAT SHOCK RESPONSE; HYDROPHOBICITY; MACROAUTOPHAGY; MALE; METAL BINDING; MOLECULAR WEIGHT; MORTALITY; MOTONEURON; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN HOMEOSTASIS; PROTEIN QUALITY; SOLUBILITY; SPINAL CORD; SURVIVAL; UPREGULATION; WEIGHT REDUCTION;

MUS;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PROTEOMICS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SPINAL CORD; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTORS;

EID: 84887963150     PISSN: None     EISSN: 17501326     Source Type: Journal    
DOI: 10.1186/1750-1326-8-43     Document Type: Article

References (80)

1. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, Hentati A, Donaldson D, Goto J, O'Regan JP, Deng HX, et al. Nature 1993 362 59 62 10.1038/362059a0 8446170 (Pubitemid 23087289)
2. TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Kabashi E, Valdmanis PN, Dion P, Spiegelman D, McConkey BJ, Vande Velde C, Bouchard JP, Lacomblez L, Pochigaeva K, Salachas F, et al. Nat Genet 2008 40 572 574 10.1038/ng.132 18372902 (Pubitemid 351601218)
3. Transgenics, toxicity and therapeutics in rodent models of mutant SOD1-mediated familial ALS. Turner BJ, Talbot K, Prog Neurobiol 2008 85 94 134 10.1016/j.pneurobio.2008.01.001 18282652
4. Copper-zinc superoxide dismutase and amyotrophic lateral sclerosis. Valentine JS, Doucette PA, Zittin Potter S, Annual review of biochemistry 2005 74 563 593 10.1146/annurev.biochem.72.121801.161647 15952898 (Pubitemid 40995518)
5. Copper and zinc metallation status of copper-zinc superoxide dismutase from amyotrophic lateral sclerosis transgenic mice. Lelie HL, Liba A, Bourassa MW, Chattopadhyay M, Chan PK, Gralla EB, Miller LM, Borchelt DR, Valentine JS, Whitelegge JP, The Journal of biological chemistry 2011 286 2795 2806 10.1074/jbc.M110.186999 21068388
6. Molecular biology of amyotrophic lateral sclerosis: insights from genetics. Pasinelli P, Brown RH, Nature reviews Neuroscience 2006 7 710 723 10.1038/nrn1971 16924260 (Pubitemid 44267495)
7. Metal deficiency increases aberrant hydrophobicity of mutant superoxide dismutases that cause amyotrophic lateral sclerosis. Tiwari A, Liba A, Sohn SH, Seetharaman SV, Bilsel O, Matthews CR, Hart PJ, Valentine JS, Hayward LJ, J Biol Chem 2009 284 27746 27758 10.1074/jbc.M109.043729 19651777
8. Aberrantly increased hydrophobicity shared by mutants of Cu, Zn-superoxide dismutase in familial amyotrophic lateral sclerosis. Tiwari A, Xu Z, Hayward LJ, J Biol Chem 2005 280 29771 29779 10.1074/jbc.M504039200 15958382 (Pubitemid 41177054)
9. Prediction of hot spots of aggregation in disease-linked polypeptides. Sanchez de Groot N, Pallares I, Aviles FX, Vendrell J, Ventura S, BMC Struct Biol 2005 5 18 10.1186/1472-6807-5-18 16197548 (Pubitemid 41457462)
10. Prediction of aggregation-prone and aggregation-susceptible regions in proteins associated with neurodegenerative diseases. Pawar AP, Dubay KF, Zurdo J, Chiti F, Vendruscolo M, Dobson CM, Journal of molecular biology 2005 350 379 392 10.1016/j.jmb.2005.04.016 15925383 (Pubitemid 40805470)
11. Factors governing the substrate recognition by GroEL chaperone: a sequence correlation approach. Chaudhuri TK, Gupta P, Cell Stress Chaperones 2005 10 24 36 10.1379/CSC-64R1.1 15832945 (Pubitemid 40446053)
12. Substrate specificity of the DnaK chaperone determined by screening cellulose-bound peptide libraries. Rudiger S, Germeroth L, Schneider-Mergener J, Bukau B, Embo J 1997 16 1501 1507 10.1093/emboj/16.7.1501 9130695 (Pubitemid 27151945)
13. Affinity panning of a library of peptides displayed on bacteriophages reveals the binding specificity of BiP. Blond-Elguindi S, Cwirla SE, Dower WJ, Lipshutz RJ, Sprang SR, Sambrook JF, Gething MJ, Cell 1993 75 717 728 10.1016/0092-8674(93)90492-9 7902213 (Pubitemid 23346370)
14. Unique peptide substrate binding properties of 110-kDa heat-shock protein (Hsp110) determine its distinct chaperone activity. Xu X, Sarbeng EB, Vorvis C, Kumar DP, Zhou L, Liu Q, J Biol Chem 2012 287 5661 5672 10.1074/jbc.M111.275057 22157767
15. From the cradle to the grave: molecular chaperones that may choose between folding and degradation. Hohfeld J, Cyr DM, Patterson C, EMBO Rep 2001 2 885 890 10.1093/embo-reports/kve206 11600451 (Pubitemid 33040574)
16. Chaperones in autophagy. Kaushik S, Cuervo AM, Pharmacol Res 2012 66 484 493 10.1016/j.phrs.2012.10.002 23059540
17. Structural and biophysical properties of the pathogenic SOD1 variant H46R/H48Q. Winkler DD, Schuermann JP, Cao X, Holloway SP, Borchelt DR, Carroll MC, Proescher JB, Culotta VC, Hart PJ, Biochemistry 2009 48 3436 3447 10.1021/bi8021735 19227972
18. A Novel Approach for Screening the Proteome for Changes in Protein Conformation. Pierce A, Dewaal E, Vanremmen H, Richardson A, Chaudhuri A, Biochemistry 2006 45 3077 3085 10.1021/bi052031i 16503663 (Pubitemid 43334556)
19. Conformational States and Protein Stability from a Proteomic Perspective. Prosinecki V, Faísca PFN, Gomes CM, Current Proteomics 2007 4 44 52 10.2174/157016407781387375 (Pubitemid 47203928)
20. Oxidation and structural perturbation of redox-sensitive enzymes in injured skeletal muscle. Pierce AP, de Waal E, McManus LM, Shireman PK, Chaudhuri AR, Free Radic Biol Med 2007 43 1584 1593 10.1016/j.freeradbiomed. 2007.08.019 18037124 (Pubitemid 350122984)
21. GAPDH is conformationally and functionally altered in association with oxidative stress in mouse models of amyotrophic lateral sclerosis. Pierce A, Mirzaei H, Muller F, De Waal E, Taylor AB, Leonard S, Van Remmen H, Regnier F, Richardson A, Chaudhuri A, J Mol Biol 2008 382 1195 1210 10.1016/j.jmb.2008.07. 088 18706911
22. New vaccine development for chronic brain disease. Barrett AD, Kayed R, Jackson GR, Cunningham KA, Neuropsychopharmacology 2010 35 354 10.1038/npp.2009.147 20010720
23. Activation of heat shock gene transcription by heat shock factor 1 involves oligomerization, acquisition of DNA-binding activity, and nuclear localization and can occur in the absence of stress. Sarge KD, Murphy SP, Morimoto RI, Mol Cell Biol 1993 13 1392 1407 8441385 (Pubitemid 23068075)
24. Treatment with arimoclomol, a coinducer of heat shock proteins, delays disease progression in ALS mice. Kieran D, Kalmar B, Dick JR, Riddoch-Contreras J, Burnstock G, Greensmith L, Nat Med 2004 10 402 405 10.1038/nm1021 15034571 (Pubitemid 38508519)
25. Arimoclomol, a coinducer of heat shock proteins for the potential treatment of amyotrophic lateral sclerosis. Phukan J, IDrugs 2010 13 482 496 20582873
26. Neuroprotective drug riluzole amplifies the heat shock factor 1 (HSF1)- and glutamate transporter 1 (GLT1)-dependent cytoprotective mechanisms for neuronal survival. Liu AY, Mathur R, Mei N, Langhammer CG, Babiarz B, Firestein BL, J Biol Chem 2011 286 2785 2794 10.1074/jbc.M110.158220 21098017
27. Riluzole increases the amount of latent HSF1 for an amplified heat shock response and cytoprotection. Yang J, Bridges K, Chen KY, Liu AY, PLoS One 2008 3 2864 10.1371/journal.pone.0002864 18682744
28. A Novel mouse model of enhanced proteostasis: Full-length human heat shock factor 1 transgenic mice. Pierce A, Wei R, Halade D, Yoo SE, Ran Q, Richardson A, Biochem Biophys Res Commun 2010 402 59 65 10.1016/j.bbrc.2010.09. 111 20920476
29. Glutamine-mediated dual regulation of heat shock transcription factor-1 activation and expression. Xue H, Slavov D, Wischmeyer PE, J Biol Chem 2012 287 40400 40413 10.1074/jbc.M112.410712 23055521
30. High threshold for induction of the stress response in motor neurons is associated with failure to activate HSF1. Batulan Z, Shinder GA, Minotti S, He BP, Doroudchi MM, Nalbantoglu J, Strong MJ, Durham HD, J Neurosci 2003 23 5789 5798 12843283 (Pubitemid 36807858)
31. Regulation of longevity in Caenorhabditis elegans by heat shock factor and molecular chaperones. Morley JF, Morimoto RI, Mol Biol Cell 2004 15 657 664 14668486 (Pubitemid 38146482)
32. The aggregation and neurotoxicity of TDP-43 and its ALS-associated 25 kDa fragment are differentially affected by molecular chaperones in Drosophila. Gregory JM, Barros TP, Meehan S, Dobson CM, Luheshi LM, PLoS One 2012 7 31899 10.1371/journal.pone.0031899 22384095
33. Over-expression of heat shock factor 1 phenocopies the effect of chronic inhibition of TOR by rapamycin and is sufficient to ameliorate Alzheimer's-like deficits in mice modeling the disease. Pierce A, Podlutskaya N, Halloran JJ, Hussong SA, Lin PY, Burbank R, Hart MJ, Galvan V, J Neurochem 2013 124 880 893 10.1111/jnc.12080 23121022
34. Active HSF1 significantly suppresses polyglutamine aggregate formation in cellular and mouse models. Fujimoto M, Takaki E, Hayashi T, Kitaura Y, Tanaka Y, Inouye S, Nakai A, J Biol Chem 2005 280 34908 34916 10.1074/jbc.M506288200 16051598 (Pubitemid 41504625)
35. Heat shock factor 1 regulates lifespan as distinct from disease onset in prion disease. Steele AD, Hutter G, Jackson WS, Heppner FL, Borkowski AW, King OD, Raymond GJ, Aguzzi A, Lindquist S, Proc Natl Acad Sci USA 2008 105 13626 13631 10.1073/pnas.0806319105 18757733
36. Over-expression of heat shock factor 1 phenocopies the effect of chronic inhibition of TOR by rapamycin and is sufficient to ameliorate Alzheimer's-like deficits in mice modeling the disease. Pierce A, Podlutskaya N, Halloran JJ, Hussong SA, Lin PY, Burbank R, Hart MJ, Galvan V, Journal of neurochemistry 2013 124 880 893 10.1111/jnc.12080 23121022
37. Optimizing separation efficiency of 2-DE procedures for visualization of different superoxide dismutase forms in a cellular model of amyotrophic lateral sclerosis. Di Poto C, Iadarola P, Salvini R, Passadore I, Cereda C, Ceroni M, Bardoni AM, Electrophoresis 2007 28 4340 4347 10.1002/elps.200700162 17987632 (Pubitemid 350259036)
38. Exposure of hydrophobic surfaces initiates aggregation of diverse ALS-causing superoxide dismutase-1 mutants. Munch C, Bertolotti A, J Mol Biol 2010 399 512 525 10.1016/j.jmb.2010.04.019 20399791
39. Structural consequences of the familial amyotrophic lateral sclerosis SOD1 mutant His46Arg. Antonyuk S, Elam JS, Hough MA, Strange RW, Doucette PA, Rodriguez JA, Hayward LJ, Valentine JS, Hart PJ, Hasnain SS, Protein Sci 2005 14 1201 1213 10.1110/ps.041256705 15840828 (Pubitemid 40577800)
40. Disease-associated mutations at copper ligand histidine residues of superoxide dismutase 1 diminish the binding of copper and compromise dimer stability. Wang J, Caruano-Yzermans A, Rodriguez A, Scheurmann JP, Slunt HH, Cao X, Gitlin J, Hart PJ, Borchelt DR, J Biol Chem 2007 282 345 352 17092942 (Pubitemid 47076602)
41. Proteins that bind to misfolded mutant superoxide dismutase-1 in spinal cords from transgenic amyotrophic lateral sclerosis (ALS) model mice. Zetterstrom P, Graffmo KS, Andersen PM, Brannstrom T, Marklund SL, J Biol Chem 2011 286 20130 20136 10.1074/jbc.M111.218842 21493711
42. Degradation of amyotrophic lateral sclerosis-linked mutant Cu, Zn-superoxide dismutase proteins by macroautophagy and the proteasome. Kabuta T, Suzuki Y, Wada K, J Biol Chem 2006 281 30524 30533 10.1074/jbc.M603337200 16920710 (Pubitemid 44582109)
43. CHIP promotes proteasomal degradation of familial ALS-linked mutant SOD1 by ubiquitinating Hsp/Hsc70. Urushitani M, Kurisu J, Tateno M, Hatakeyama S, Nakayama K, Kato S, Takahashi R, J Neurochem 2004 90 231 244 10.1111/j.1471-4159.2004.02486.x 15198682 (Pubitemid 38879177)
44. Amyotrophic lateral sclerosis is a non-amyloid disease in which extensive misfolding of SOD1 is unique to the familial form. Kerman A, Liu HN, Croul S, Bilbao J, Rogaeva E, Zinman L, Robertson J, Chakrabartty A, Acta Neuropathol 2010 119 335 344 10.1007/s00401-010-0646-5 20111867
45. Aberrant localization of FUS and TDP43 is associated with misfolding of SOD1 in amyotrophic lateral sclerosis. Pokrishevsky E, Grad LI, Yousefi M, Wang J, Mackenzie IR, Cashman NR, PloS one 2012 7 35050 10.1371/journal.pone.0035050 22493728
46. ANS binding reveals common features of cytotoxic amyloid species. Bolognesi B, Kumita JR, Barros TP, Esbjorner EK, Luheshi LM, Crowther DC, Wilson MR, Dobson CM, Favrin G, Yerbury JJ, ACS Chem Biol 2010 5 735 740 10.1021/cb1001203 20550130
47. DNA and RNA strand scission by copper, zinc and manganese superoxide dismutases. Dowjat WK, Kharatishvili M, Costa M, Biometals: an international journal on the role of metal ions in biology, biochemistry, and medicine 1996 9 327 335 (Pubitemid 26394805)
48. DNA is a template for accelerating the aggregation of copper, zinc superoxide dismutase. Jiang W, Han Y, Zhou R, Zhang L, Liu C, Biochemistry 2007 46 5911 5923 10.1021/bi062234m 17469801 (Pubitemid 46799154)
49. Mutant copper-zinc superoxide dismutase binds to and destabilizes human low molecular weight neurofilament mRNA. Ge WW, Wen W, Strong W, Leystra-Lantz C, Strong MJ, The Journal of biological chemistry 2005 280 118 124 15507437 (Pubitemid 40164972)
50. Amyotrophic lateral sclerosis-linked mutant SOD1 sequesters Hu antigen R (HuR) and TIA-1-related protein (TIAR): implications for impaired post-transcriptional regulation of vascular endothelial growth factor. Lu L, Wang S, Zheng L, Li X, Suswam EA, Zhang X, Wheeler CG, Nabors LB, Filippova N, King PH, The Journal of biological chemistry 2009 284 33989 33998 10.1074/jbc.M109.067918 19805546
51. Characterization of detergent-insoluble proteins in ALS indicates a causal link between nitrative stress and aggregation in pathogenesis. Basso M, Samengo G, Nardo G, Massignan T, D'Alessandro G, Tartari S, Cantoni L, Marino M, Cheroni C, De Biasi S, et al. PloS one 2009 4 8130 10.1371/journal.pone.0008130 19956584
52. Proteins with neomorphic moonlighting functions in disease. Jeffery CJ, IUBMB Life 2011 63 489 494 10.1002/iub.504 21698752
53. Impaired glucose tolerance in patients with amyotrophic lateral sclerosis. Pradat PF, Bruneteau G, Gordon PH, Dupuis L, Bonnefont-Rousselot D, Simon D, Salachas F, Corcia P, Frochot V, Lacorte JM, et al. Amyotroph Lateral Scler 2010 11 166 171 10.3109/17482960902822960 20184518
54. The metabolic hypothesis in amyotrophic lateral sclerosis: insights from mutant Cu/Zn-superoxide dismutase mice. de Aguilar JL G, Dupuis L, Oudart H, Loeffler JP, Biomed Pharmacother 2005 59 190 196 10.1016/j.biopha.2005.03.003 15862714 (Pubitemid 40603332)
55. Clinical aspects and pathology of Alexander disease, and morphological and functional alteration of astrocytes induced by GFAP mutation. Yoshida T, Nakagawa M, Neuropathology 2012 32 440 446 10.1111/j.1440-1789.2011.01268.x 22118268
56. Chaperone networks: tipping the balance in protein folding diseases. Voisine C, Pedersen JS, Morimoto RI, Neurobiology of disease 2010 40 12 20 10.1016/j.nbd.2010.05.007 20472062
57. Conformational lability of two molecular chaperones Hsc70 and gp96: effects of pH and temperature. Fan H, Kashi RS, Middaugh CR, Archives of biochemistry and biophysics 2006 447 34 45 10.1016/j.abb.2006.01.012 16487475
58. The role of immunophilins in mutant superoxide dismutase-1linked familial amyotrophic lateral sclerosis. Lee JP, Palfrey HC, Bindokas VP, Ghadge GD, Ma L, Miller RJ, Roos RP, Proceedings of the National Academy of Sciences of the United States of America 1999 96 3251 3256 10.1073/pnas.96.6.3251 10077670 (Pubitemid 29148877)
59. Intragenic deletion in the gene encoding ubiquitin carboxy-terminal hydrolase in gad mice. Saigoh K, Wang YL, Suh JG, Yamanishi T, Sakai Y, Kiyosawa H, Harada T, Ichihara N, Wakana S, Kikuchi T, Wada K, Nat Genet 1999 23 47 51 10471497 (Pubitemid 29418786)
60. UCHL1 (PGP 9.5): neuronal biomarker and ubiquitin system protein. Day IN, Thompson RJ, Prog Neurobiol 2010 90 327 362 10.1016/j.pneurobio.2009.10.020 19879917
61. The UCH-L1 gene encodes two opposing enzymatic activities that affect alpha-synuclein degradation and Parkinson's disease susceptibility. Liu Y, Fallon L, Lashuel HA, Liu Z, Lansbury PT Jr, Cell 2002 111 209 218 10.1016/S0092-8674(02)01012-7 12408865 (Pubitemid 35292441)
62. 14-3-3 proteins in neurodegeneration. Steinacker P, Aitken A, Otto M, Seminars in cell & developmental biology 2011 22 696 704 10.1016/j.semcdb.2011.08.005 21920445
63. 14-3-3 protein binds to the low molecular weight neurofilament (NFL) mRNA 3' UTR. Ge WW, Volkening K, Leystra-Lantz C, Jaffe H, Strong MJ, Molecular and cellular neurosciences 2007 34 80 87 10.1016/j.mcn.2006.10.001 17098443 (Pubitemid 46026930)
64. Identification of novel 14-3-3zeta interacting proteins by quantitative immunoprecipitation combined with knockdown (QUICK). Ge F, Li WL, Bi LJ, Tao SC, Zhang ZP, Zhang XE, J Proteome Res 2010 9 5848 5858 10.1021/pr100616g 20879785
65. Bioinformatic and experimental survey of 14-3-3-binding sites. Johnson C, Crowther S, Stafford MJ, Campbell DG, Toth R, MacKintosh C, The Biochemical journal 2010 427 69 78 10.1042/BJ20091834 20141511
66. Effect of mutations mimicking phosphorylation on the structure and properties of human 14-3-3zeta. Sluchanko NN, Chernik IS, Seit-Nebi AS, Pivovarova AV, Levitsky DI, Gusev NB, Archives of biochemistry and biophysics 2008 477 305 312 10.1016/j.abb.2008.05.020 18559254
67. Serine 58 of 14-3-3zeta is a molecular switch regulating ASK1 and oxidant stress-induced cell death. Zhou J, Shao Z, Kerkela R, Ichijo H, Muslin AJ, Pombo C, Force T, Molecular and cellular biology 2009 29 4167 4176 10.1128/MCB.01067-08 19451227
68. Cytosolic proteins lose solubility as amyloid deposits in a transgenic mouse model of Alzheimer-type amyloidosis. Xu G, Stevens SM Jr, Moore BD, McClung S, Borchelt DR, Hum Mol Genet 2013 22 2765 2774 10.1093/hmg/ddt121 23512986
69. Pseudophosphorylated alphaB-crystallin is a nuclear chaperone imported into the nucleus with help of the SMN complex. den Engelsman J, van de Schootbrugge C, Yong J, Pruijn GJ, Boelens WC, PLoS One 2013 8 73489 10.1371/journal.pone.0073489 24023879
70. Interaction between alphaB-crystallin and the human 20S proteasomal subunit C8/alpha7. Boelens WC, Croes Y, de Jong WW, Biochim Biophys Acta 2001 1544 311 319 10.1016/S0167-4838(00)00243-0 11341940 (Pubitemid 32121869)
71. Transgenic mouse models of amyotrophic lateral sclerosis. Julien JP, Kriz J, Biochim Biophys Acta 2006 1762 1013 1024 10.1016/j.bbadis.2006.03.006 16675207 (Pubitemid 44750574)
72. Non-cell autonomous toxicity in neurodegenerative disorders: ALS and beyond. Ilieva H, Polymenidou M, Cleveland DW, J Cell Biol 2009 187 761 772 10.1083/jcb.200908164 19951898
73. Mutant SOD1 in cell types other than motor neurons and oligodendrocytes accelerates onset of disease in ALS mice. Yamanaka K, Boillee S, Roberts EA, Garcia ML, McAlonis-Downes M, Mikse OR, Cleveland DW, Goldstein LS, Proc Natl Acad Sci USA 2008 105 7594 7599 10.1073/pnas.0802556105 18492803 (Pubitemid 351830063)
74. Onset and progression in inherited ALS determined by motor neurons and microglia. Boillee S, Yamanaka K, Lobsiger CS, Copeland NG, Jenkins NA, Kassiotis G, Kollias G, Cleveland DW, Science 2006 312 1389 1392 10.1126/science.1123511 16741123 (Pubitemid 43839552)
75. Fibrillar inclusions and motor neuron degeneration in transgenic mice expressing superoxide dismutase 1 with a disrupted copper-binding site. Wang J, Xu G, Gonzales V, Coonfield M, Fromholt D, Copeland NG, Jenkins NA, Borchelt DR, Neurobiology of disease 2002 10 128 138 10.1006/nbdi.2002.0498 12127151 (Pubitemid 34775466)
76. Antisense oligonucleotide therapy for neurodegenerative disease. Smith RA, Miller TM, Yamanaka K, Monia BP, Condon TP, Hung G, Lobsiger CS, Ward CM, McAlonis-Downes M, Wei H, et al. J Clin Invest 2006 116 2290 2296 10.1172/JCI25424 16878173 (Pubitemid 44162339)
77. Human neural stem cell replacement therapy for amyotrophic lateral sclerosis by spinal transplantation. Hefferan MP, Galik J, Kakinohana O, Sekerkova G, Santucci C, Marsala S, Navarro R, Hruska-Plochan M, Johe K, Feldman E, et al. PLoS One 2012 7 42614 10.1371/journal.pone.0042614 22916141
78. Protein conformational changes induced by 1,1'-bis(4-anilino-5- naphthalenesulfonic acid): preferential binding to the molten globule of DnaK. Shi L, Palleros DR, Fink AL, Biochemistry 1994 33 7536 7546 10.1021/bi00190a006 8011619 (Pubitemid 24230577)
79. AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. Trott O, Olson AJ, J Comput Chem 2010 31 455 461 19499576
80. Structural basis for conformational plasticity of the Parkinson's disease-associated ubiquitin hydrolase UCH-L1. Das C, Hoang QQ, Kreinbring CA, Luchansky SJ, Meray RK, Ray SS, Lansbury PT, Ringe D, Petsko GA, Proceedings of the National Academy of Sciences of the United States of America 2006 103 4675 4680 10.1073/pnas.0510403103 16537382