ALS-linked protein disulfide isomerase variants cause motor dysfunction

EMBO Journal

Volumn 35, Issue 8, 2016, Pages 845-865

  Woehlbier, Ute ^a,b,c   Colombo, Alicia ^b,d   Saaranen, Mirva J ^e   Pérez, Viviana ^f   Ojeda, Jorge ^f   Bustos, Fernando J ^g   Andreu, Catherine I ^a,b   Torres, Mauricio ^a,b   Valenzuela, Vicente ^a,b,h   Medinas, Danilo B ^a,b,h   Rozas, Pablo ^a,b   Vidal, Rene L ^a,h,i   Lopez Gonzalez, Rodrigo ^j   Salameh, Johnny ^j   Fernandez Collemann, Sara ^k   Muñoz, Natalia ^a,h,i   Matus, Soledad ^a,h,i   Armisen, Ricardo ^b   Sagredo, Alfredo ^b   Palma, Karina ^a,b   Irrazabal, Thergiory ^a,b   Almeida, Sandra ^j   Gonzalez Perez, Paloma ^j   Campero, Mario ^a,l   Gao, Fen Biao ^j   Henny, Pablo ^k   Van Zundert, Brigitte ^g   Ruddock, Lloyd W ^e   Concha, Miguel L ^a,b,h   Henriquez, Juan P ^f   Brown, Robert H ^j   Hetz, Claudio ^a,b,h,m   more..

^a UNIVERSITY OF CHILE   (Chile)

^b UNIVERSITY OF CHILE   (Chile)

^c UNIVERSIDAD MAYOR   (Chile)

^d HOSPITAL CLÍNICO UNIVERSIDAD DE CHILE   (Chile)

^e UNIVERSITY OF OULU   (Finland)

^f UNIVERSITY OF CONCEPCIÓN   (Chile)

^g UNIVERSIDAD ANDRÉS BELLO   (Chile)

^h Universidad de Chile and Geroscience Center for Brain Health and Metabolism   (Chile)

ⁱ Millennium Nucleus for Regenerative Biology and Neurounion Biomedical Foundation   (Chile)

^j UNIVERSITY OF MASSACHUSETTS   (United States)

^k PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^l UNIVERSIDAD DEL DESARROLLO   (Chile)

^m HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

more..

Author keywords

amyotrophic lateral sclerosis; ERp57; PDIA1; protein disulfide isomerase

Indexed keywords

PROTEIN DISULFIDE ISOMERASE; PROTEIN DISULFIDE ISOMERASE A1; PROTEIN DISULFIDE ISOMERASE A3; UNCLASSIFIED DRUG; P4HB PROTEIN, HUMAN; PDIA3 PROTEIN, HUMAN; PDIA3 PROTEIN, MOUSE; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; DOPAMINERGIC NERVE CELL; EMBRYO; GENE EXPRESSION; GENE MUTATION; GENETIC RISK; MOTONEURON; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; MOUSE; MUSCLE DENERVATION; NERVE FIBER GROWTH; NEUROMUSCULAR SYNAPSE; NONHUMAN; PATHOGENICITY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN HOMEOSTASIS; WILD TYPE; ZEBRA FISH; ANIMAL; ELECTROMYOGRAPHY; EMBRYOLOGY; ENDOPLASMIC RETICULUM STRESS; GENETICS; HUMAN; KNOCKOUT MOUSE; METABOLISM; MUTATION; NEURITE; NONMAMMALIAN EMBRYO; PATHOLOGY; TRANSGENIC ANIMAL;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; ELECTROMYOGRAPHY; EMBRYO, NONMAMMALIAN; ENDOPLASMIC RETICULUM STRESS; HUMANS; MICE, KNOCKOUT; MOTOR NEURONS; MUTATION; NEURITES; PROCOLLAGEN-PROLINE DIOXYGENASE; PROTEIN DISULFIDE-ISOMERASES; ZEBRAFISH;

EID: 84958594182     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201592224     Document Type: Article

References (99)

1. Andreu CI, Woehlbier U, Torres M, Hetz C, (2012) Protein disulfide isomerases in neurodegeneration: from disease mechanisms to biomedical applications. FEBS Lett 586: 2826-2834
2. Appenzeller-Herzog C, Riemer J, Zito E, Chin KT, Ron D, Spiess M, Ellgaard L, (2010) Disulphide production by Ero1alpha-PDI relay is rapid and effectively regulated. EMBO J 29: 3318-3329
3. Armstrong GA, Drapeau P, (2013) Loss and gain of FUS function impair neuromuscular synaptic transmission in a genetic model of ALS. Hum Mol Genet 22: 4282-4292
4. Atkin JD, Farg MA, Turner BJ, Tomas D, Lysaght JA, Nunan J, Rembach A, Nagley P, Beart PM, Cheema SS, Horne MK, (2006) Induction of the unfolded protein response in familial amyotrophic lateral sclerosis and association of protein-disulfide isomerase with superoxide dismutase 1. J Biol Chem 281: 30152-30165
5. Atkin JD, Farg MA, Walker AK, McLean C, Tomas D, Horne MK, (2008) Endoplasmic reticulum stress and induction of the unfolded protein response in human sporadic amyotrophic lateral sclerosis. Neurobiol Dis 30: 400-407
6. Babin PJ, Goizet C, Raldua D, (2014) Zebrafish models of human motor neuron diseases: advantages and limitations. Prog Neurobiol 118: 36-58
7. Bernard-Marissal N, Sunyach C, Marissal T, Raoul C, Pettmann B, (2014) Calreticulin levels determine onset of early muscle denervation by fast motoneurons of ALS model mice. Neurobiol Dis 73: 130-136
8. Bernard-Marissal N, Sunyach C, Marissal T, Raoul C, Pettmann B, (2015) Calreticulin levels determine onset of early muscle denervation by fast motoneurons of ALS model mice. Neurobiol Dis 73: 130-136
9. Castillo V, Onate M, Woehlbier U, Rozas P, Andreu C, Medinas D, Valdes P, Osorio F, Mercado G, Vidal RL, Kerr B, Court FA, Hetz C, (2015) Functional Role of the Disulfide Isomerase ERp57 in Axonal Regeneration. PLoS One 10: e0136620
10. Chen H, Qian K, Du Z, Cao J, Petersen A, Liu H, Blackbourn LWT, Huang CL, Errigo A, Yin Y, Lu J, Ayala M, Zhang SC, (2014) Modeling ALS with iPSCs reveals that mutant SOD1 misregulates neurofilament balance in motor neurons. Cell Stem Cell 14: 796-809
11. Di Giorgio FP, Boulting GL, Bobrowicz S, Eggan KC, (2008) Human embryonic stem cell-derived motor neurons are sensitive to the toxic effect of glial cells carrying an ALS-causing mutation. Cell Stem Cell 3: 637-648
12. Dong G, Wearsch PA, Peaper DR, Cresswell P, Reinisch KM, (2009) Insights into MHC class I peptide loading from the structure of the tapasin-ERp57 thiol oxidoreductase heterodimer. Immunity 30: 21-32
13. Douglas PM, Dillin A, (2010) Protein homeostasis and aging in neurodegeneration. J Cell Biol 190: 719-729
14. Dupuis L, Gonzalez de Aguilar JL, Echaniz-Laguna A, Eschbach J, Rene F, Oudart H, Halter B, Huze C, Schaeffer L, Bouillaud F, Loeffler JP, (2009) Muscle mitochondrial uncoupling dismantles neuromuscular junction and triggers distal degeneration of motor neurons. PLoS One 4: e5390
15. Ellgaard L, Ruddock LW, (2005) The human protein disulphide isomerase family: substrate interactions and functional properties. EMBO Rep 6: 28-32
16. Enyedi B, Varnai P, Geiszt M, (2010) Redox state of the endoplasmic reticulum is controlled by Ero1L-alpha and intraluminal calcium. Antioxid Redox Signal 13: 721-729
17. Farg MA, Soo KY, Walker AK, Pham H, Orian J, Horne MK, Warraich ST, Williams KL, Blair IP, Atkin JD, (2012) Mutant FUS induces endoplasmic reticulum stress in amyotrophic lateral sclerosis and interacts with protein disulfide-isomerase. Neurobiol Aging 33: 2855-2868
18. Feige MJ, Hendershot LM, (2011) Disulfide bonds in ER protein folding and homeostasis. Curr Opin Cell Biol 23: 167-175
19. Ferraiuolo L, Kirby J, Grierson AJ, Sendtner M, Shaw PJ, (2011) Molecular pathways of motor neuron injury in amyotrophic lateral sclerosis. Nat Rev Neurol 7: 616-630
20. Filezac de L'Etang A, Maharjan N, Cordeiro Brana M, Ruegsegger C, Rehmann R, Goswami A, Roos A, Troost D, Schneider BL, Weis J, Saxena S, (2015) Marinesco-Sjogren syndrome protein SIL1 regulates motor neuron subtype-selective ER stress in ALS. Nat Neurosci 18: 227-238
21. Fritz E, Izaurieta P, Weiss A, Mir FR, Rojas P, Gonzalez D, Rojas F, Brown RH, Madrid R, van Zundert B, (2013) Mutant SOD1-expressing astrocytes release toxic factors that trigger motor neuron death by inducing hyper-excitability. J Neurophysiol 109: 2803-2814
22. Garbi N, Tanaka S, Momburg F, Hammerling GJ, (2006) Impaired assembly of the major histocompatibility complex class I peptide-loading complex in mice deficient in the oxidoreductase ERp57. Nat Immunol 7: 93-102
23. Gonzalez-Perez P, Woehlbier U, Chian RJ, Sapp P, Rouleau GA, Leblond CS, Daoud H, Dion PA, Landers JE, Hetz C, Brown RH, (2015) Identification of rare protein disulfide isomerase gene variants in amyotrophic lateral sclerosis patients. Gene 566: 158-165
24. Grek C, Townsend DM, (2014) Protein disulfide isomerase superfamily in disease and the regulation of apoptosis. Endoplasmic Reticulum Stress Dis 1: 4-17
25. Hahm E, Li J, Kim K, Huh S, Rogelj S, Cho J, (2013) Extracellular protein disulfide isomerase regulates ligand-binding activity of alphaMbeta2 integrin and neutrophil recruitment during vascular inflammation. Blood 121: 3789-3800, S3781-3715
26. Hatahet F, Ruddock LW, (2009) Protein disulfide isomerase: a critical evaluation of its function in disulfide bond formation. Antioxid Redox Signal 11: 2807-2850
27. Haubensak W, Narz F, Heumann R, Lessmann V, (1998) BDNF-GFP containing secretory granules are localized in the vicinity of synaptic junctions of cultured cortical neurons. J Cell Sci 111 (Pt 11): 1483-1493
28. Hetz C, Bernasconi P, Fisher J, Lee AH, Bassik MC, Antonsson B, Brandt GS, Iwakoshi NN, Schinzel A, Glimcher LH, Korsmeyer SJ, (2006) Proapoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1alpha. Science 312: 572-576
29. Hetz C, Lee AH, Gonzalez-Romero D, Thielen P, Castilla J, Soto C, Glimcher LH, (2008) Unfolded protein response transcription factor XBP-1 does not influence prion replication or pathogenesis. Proc Natl Acad Sci USA 105: 757-762
30. Hetz C, Thielen P, Matus S, Nassif M, Court F, Kiffin R, Martinez G, Cuervo AM, Brown RH, Glimcher LH, (2009) XBP-1 deficiency in the nervous system protects against amyotrophic lateral sclerosis by increasing autophagy. Genes Dev 23: 2294-2306
31. Hetz C, (2012) The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol 13: 89-102
32. Hetz C, Chevet E, Harding H, (2013) Targeting the unfolded protein response in disease. Nat Rev Drug Discov 12: 703-719
33. Hetz C, Mollereau B, (2014) Disturbance of endoplasmic reticulum proteostasis in neurodegenerative diseases. Nat Rev Neurosci 15: 233-249
34. Hirsch I, Weiwad M, Prell E, Ferrari DM, (2014) ERp29 deficiency affects sensitivity to apoptosis via impairment of the ATF6-CHOP pathway of stress response. Apoptosis 19: 801-815
35. Hoffstrom BG, Kaplan A, Letso R, Schmid RS, Turmel GJ, Lo DC, Stockwell BR, (2010) Inhibitors of protein disulfide isomerase suppress apoptosis induced by misfolded proteins. Nat Chem Biol 6: 900-906
36. Honjo Y, Kaneko S, Ito H, Horibe T, Nagashima M, Nakamura M, Fujita K, Takahashi R, Kusaka H, Kawakami K, (2011) Protein disulfide isomerase-immunopositive inclusions in patients with amyotrophic lateral sclerosis. Amyotroph Lateral Scler 12: 444-450
37. Hosoda A, Tokuda M, Akai R, Kohno K, Iwawaki T, (2010) Positive contribution of ERdj5/JPDI to endoplasmic reticulum protein quality control in the salivary gland. Biochem J 425: 117-125
38. Ilieva EV, Ayala V, Jove M, Dalfo E, Cacabelos D, Povedano M, Bellmunt MJ, Ferrer I, Pamplona R, Portero-Otin M, (2007) Oxidative and endoplasmic reticulum stress interplay in sporadic amyotrophic lateral sclerosis. Brain 130: 3111-3123
39. Jaronen M, Goldsteins G, Koistinaho J, (2014) ER stress and unfolded protein response in amyotrophic lateral sclerosis-a controversial role of protein disulphide isomerase. Front Cell Neurosci 8: 402
40. Jessop CE, Chakravarthi S, Garbi N, Hammerling GJ, Lovell S, Bulleid NJ, (2007) ERp57 is essential for efficient folding of glycoproteins sharing common structural domains. EMBO J 26: 28-40
41. Jessop CE, Watkins RH, Simmons JJ, Tasab M, Bulleid NJ, (2009) Protein disulphide isomerase family members show distinct substrate specificity: P5 is targeted to BiP client proteins. J Cell Sci 122: 4287-4295
42. Jiang M, Chen G, (2006) High Ca2+-phosphate transfection efficiency in low-density neuronal cultures. Nat Protoc 1: 695-700
43. Jin H, Mimura N, Kashio M, Koseki H, Aoe T, (2014) Late-onset of spinal neurodegeneration in knock-in mice expressing a mutant BiP. PLoS One 9: e112837
44. Kabashi E, Lin L, Tradewell ML, Dion PA, Bercier V, Bourgouin P, Rochefort D, Bel Hadj S, Durham HD, Vande Velde C, Rouleau GA, Drapeau P, (2009) Gain and loss of function of ALS-related mutations of TARDBP (TDP-43) cause motor deficits in vivo. Hum Mol Genet 19: 671-683
45. Kabashi E, Champagne N, Brustein E, Drapeau P, (2010) In the swim of things: recent insights to neurogenetic disorders from zebrafish. Trends Genet 26: 373-381
46. Kabashi E, Bercier V, Lissouba A, Liao M, Brustein E, Rouleau GA, Drapeau P, (2011) FUS and TARDBP but not SOD1 interact in genetic models of amyotrophic lateral sclerosis. PLoS Genet 7: e1002214
47. Karala AR, Lappi AK, Saaranen MJ, Ruddock LW, (2009) Efficient peroxide-mediated oxidative refolding of a protein at physiological pH and implications for oxidative folding in the endoplasmic reticulum. Antioxid Redox Signal 11: 963-970
48. Kiskinis E, Sandoe J, Williams LA, Boulting GL, Moccia R, Wainger BJ, Han S, Peng T, Thams S, Mikkilineni S, Mellin C, Merkle FT, Davis-Dusenbery BN, Ziller M, Oakley D, Ichida J, Di Costanzo S, Atwater N, Maeder ML, Goodwin MJ, et al, (2014) Pathways disrupted in human ALS motor neurons identified through genetic correction of mutant SOD1. Cell Stem Cell 14: 781-795
49. Klein A, Mosqueira M, Martinez G, Robledo F, Gonzalez M, Caballero B, Cancino GI, Alvarez AR, Hetz C, Zanlungo S, (2011) Lack of activation of the unfolded protein response in mouse and cellular models of Niemann-Pick type C disease. Neurodegener Dis 8: 124-128
50. Kozlov G, Maattanen P, Schrag JD, Pollock S, Cygler M, Nagar B, Thomas DY, Gehring K, (2006) Crystal structure of the bb' domains of the protein disulfide isomerase ERp57. Structure 14: 1331-1339
51. Kraus A, Groenendyk J, Bedard K, Baldwin TA, Krause KH, Dubois-Dauphin M, Dyck J, Rosenbaum EE, Korngut L, Colley NJ, Gosgnach S, Zochodne D, Todd K, Agellon LB, Michalak M, (2010) Calnexin deficiency leads to dysmyelination. J Biol Chem 285: 18928-18938
52. Kwok CT, Morris AG, Frampton J, Smith B, Shaw CE, de Belleroche J, (2013) Association studies indicate that protein disulfide isomerase is a risk factor in amyotrophic lateral sclerosis. Free Radic Biol Med 58: 81-86
53. Lappi AK, Lensink MF, Alanen HI, Salo KE, Lobell M, Juffer AH, Ruddock LW, (2004) A conserved arginine plays a role in the catalytic cycle of the protein disulphide isomerases. J Mol Biol 335: 283-295
54. Leblond CS, Kaneb HM, Dion PA, Rouleau GA, (2014) Dissection of genetic factors associated with amyotrophic lateral sclerosis. Exp Neurol 262 Pt B: 91-101
55. Lee YB, Chen HJ, Peres JN, Gomez-Deza J, Attig J, Stalekar M, Troakes C, Nishimura AL, Scotter EL, Vance C, Adachi Y, Sardone V, Miller JW, Smith BN, Gallo JM, Ule J, Hirth F, Rogelj B, Houart C, Shaw CE, (2013) Hexanucleotide repeats in ALS/FTD form length-dependent RNA foci, sequester RNA binding proteins, and are neurotoxic. Cell Rep 5: 1178-1186
56. Li Y, Camacho P, (2004) Ca2+-dependent redox modulation of SERCA 2b by ERp57. J Cell Biol 164: 35-46
57. Ling SC, Polymenidou M, Cleveland DW, (2013) Converging Mechanisms in ALS and FTD: disrupted RNA and Protein Homeostasis. Neuron 79: 416-438
58. Lisbona F, Rojas-Rivera D, Thielen P, Zamorano S, Todd D, Martinon F, Glavic A, Kress C, Lin JH, Walter P, Reed JC, Glimcher LH, Hetz C, (2009) BAX inhibitor-1 is a negative regulator of the ER stress sensor IRE1alpha. Mol Cell 33: 679-691
59. Liu JX, Brannstrom T, Andersen PM, Pedrosa-Domellof F, (2013) Distinct changes in synaptic protein composition at neuromuscular junctions of extraocular muscles versus limb muscles of ALS donors. PLoS One 8: e57473
60. Lopez-Gonzalez R, Kunckles P, Velasco I, (2009) Transient recovery in a rat model of familial amyotrophic lateral sclerosis after transplantation of motor neurons derived from mouse embryonic stem cells. Cell Transplant 18: 1171-1181
61. Ma T, Trinh MA, Wexler AJ, Bourbon C, Gatti E, Pierre P, Cavener DR, Klann E, (2013) Suppression of eIF2alpha kinases alleviates Alzheimer's disease-related plasticity and memory deficits. Nat Neurosci 16: 1299-1305
62. Maattanen P, Gehring K, Bergeron JJ, Thomas DY, (2010) Protein quality control in the ER: the recognition of misfolded proteins. Semin Cell Dev Biol 21: 500-511
63. Mardones P, Martinez G, Hetz C, (2015) Control of systemic proteostasis by the nervous system. Trends Cell Biol 25: 1-10
64. Matus S, Lopez E, Valenzuela V, Nassif M, Hetz C, (2013b) Functional contribution of the transcription factor ATF4 to the pathogenesis of amyotrophic lateral sclerosis. PLoS One 8: e66672
65. Matus S, Medinas DB, Hetz C, (2014) Common ground: stem cell approaches find shared pathways underlying ALS. Cell Stem Cell 14: 697-699
66. Matus S, Valenzuela V, Medinas DB, Hetz C, (2013a) ER dysfunction and protein folding stress in ALS. Int J Cell Biol 2013: 674751
67. Moreno JA, Radford H, Peretti D, Steinert JR, Verity N, Martin MG, Halliday M, Morgan J, Dinsdale D, Ortori CA, Barrett DA, Tsaytler P, Bertolotti A, Willis AE, Bushell M, Mallucci GR, (2012) Sustained translational repression by eIF2alpha-P mediates prion neurodegeneration. Nature 485: 507-511
68. Nagai M, Re DB, Nagata T, Chalazonitis A, Jessell TM, Wichterle H, Przedborski S, (2007) Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat Neurosci 10: 615-622
69. Nardo G, Pozzi S, Pignataro M, Lauranzano E, Spano G, Garbelli S, Mantovani S, Marinou K, Papetti L, Monteforte M, Torri V, Paris L, Bazzoni G, Lunetta C, Corbo M, Mora G, Bendotti C, Bonetto V, (2011) Amyotrophic lateral sclerosis multiprotein biomarkers in peripheral blood mononuclear cells. PLoS One 6: e25545
70. Nemere I, Garbi N, Hammerling GJ, Khanal RC, (2010) Intestinal cell calcium uptake and the targeted knockout of the 1,25D3-MARRS (membrane-associated, rapid response steroid-binding) receptor/PDIA3/Erp57. J Biol Chem 285: 31859-31866
71. Nguyen VD, Wallis K, Howard MJ, Haapalainen AM, Salo KE, Saaranen MJ, Sidhu A, Wierenga RK, Freedman RB, Ruddock LW, Williamson RA, (2008) Alternative conformations of the x region of human protein disulphide-isomerase modulate exposure of the substrate binding b' domain. J Mol Biol 383: 1144-1155
72. Oakes SA, Papa FR, (2015) The role of endoplasmic reticulum stress in human pathology. Annu Rev Pathol 10: 173-194
73. Park SW, Zhen G, Verhaeghe C, Nakagami Y, Nguyenvu LT, Barczak AJ, Killeen N, Erle DJ, (2009) The protein disulfide isomerase AGR2 is essential for production of intestinal mucus. Proc Natl Acad Sci USA 106: 6950-6955
74. Patten SA, Armstrong GA, Lissouba A, Kabashi E, Parker JA, Drapeau P, (2014) Fishing for causes and cures of motor neuron disorders. Dis Model Mech 7: 799-809
75. Perez-Garcia MJ, Burden SJ, (2012) Increasing MuSK activity delays denervation and improves motor function in ALS mice. Cell Rep 2: 497-502
76. Peters OM, Ghasemi M, Brown RH Jr, (2015) Emerging mechanisms of molecular pathology in ALS. J Clin Invest 125: 1767-1779
77. Pollock S, Kozlov G, Pelletier MF, Trempe JF, Jansen G, Sitnikov D, Bergeron JJ, Gehring K, Ekiel I, Thomas DY, (2004) Specific interaction of ERp57 and calnexin determined by NMR spectroscopy and an ER two-hybrid system. EMBO J 23: 1020-1029
78. Prudencio M, Belzil VV, Batra R, Ross CA, Gendron TF, Pregent LJ, Murray ME, Overstreet KK, Piazza-Johnston AE, Desaro P, Bieniek KF, DeTure M, Lee WC, Biendarra SM, Davis MD, Baker MC, Perkerson RB, van Blitterswijk M, Stetler CT, Rademakers R, et al, (2015) Distinct brain transcriptome profiles in C9orf72-associated and sporadic ALS. Nat Neurosci 18: 1175-1182
79. Ramirez OA, Vidal RL, Tello JA, Vargas KJ, Kindler S, Hartel S, Couve A, (2009) Dendritic assembly of heteromeric gamma-aminobutyric acid type B receptor subunits in hippocampal neurons. J Biol Chem 284: 13077-13085
80. Roussel BD, Kruppa AJ, Miranda E, Crowther DC, Lomas DA, Marciniak SJ, (2013) Endoplasmic reticulum dysfunction in neurological disease. Lancet Neurol 12: 105-118
81. Rutkevich LA, Cohen-Doyle MF, Brockmeier U, Williams DB, (2010) Functional relationship between protein disulfide isomerase family members during the oxidative folding of human secretory proteins. Mol Biol Cell 21: 3093-3105
82. Rutkevich LA, Williams DB, (2011) Participation of lectin chaperones and thiol oxidoreductases in protein folding within the endoplasmic reticulum. Curr Opin Cell Biol 23: 157-166
83. Sato T, Takahoko M, Okamoto H, (2006) HuC:Kaede, a useful tool to label neural morphologies in networks in vivo. Genesis 44: 136-142
84. Saxena S, Cabuy E, Caroni P, (2009) A role for motoneuron subtype-selective ER stress in disease manifestations of FALS mice. Nat Neurosci 12: 627-636
85. Sepulveda FJ, Bustos FJ, Inostroza E, Zuniga FA, Neve RL, Montecino M, van Zundert B, (2010) Differential roles of NMDA Receptor Subtypes NR2A and NR2B in dendritic branch development and requirement of RasGRF1. J Neurophysiol 103: 1758-1770
86. Silvennoinen L, Myllyharju J, Ruoppolo M, Orru S, Caterino M, Kivirikko KI, Koivunen P, (2004) Identification and characterization of structural domains of human ERp57: association with calreticulin requires several domains. J Biol Chem 279: 13607-13615
87. Tavender TJ, Bulleid NJ, (2010) Molecular mechanisms regulating oxidative activity of the Ero1 family in the endoplasmic reticulum. Antioxid Redox Signal 13: 1177-1187
88. Torres M, Medinas DB, Matamala JM, Woehlbier U, Cornejo VH, Solda T, Andreu C, Rozas P, Matus S, Munoz N, Vergara C, Cartier L, Soto C, Molinari M, Hetz C, (2015) The protein-disulfide isomerase ERp57 regulates the steady-state levels of the prion protein. J Biol Chem 290: 23631-23645
89. Turano C, Gaucci E, Grillo C, Chichiarelli S, (2011) ERp57/GRP58: a protein with multiple functions. Cell Mol Biol Lett 16: 539-563
90. Turner MR, Hardiman O, Benatar M, Brooks BR, Chio A, de Carvalho M, Ince PG, Lin C, Miller RG, Mitsumoto H, Nicholson G, Ravits J, Shaw PJ, Swash M, Talbot K, Traynor BJ, Van den Berg LH, Veldink JH, Vucic S, Kiernan MC, (2013) Controversies and priorities in amyotrophic lateral sclerosis. Lancet Neurol 12: 310-322
91. Valenzuela V, Collyer E, Armentano D, Parsons GB, Court FA, Hetz C, (2012) Activation of the unfolded protein response enhances motor recovery after spinal cord injury. Cell Death Dis 3: e272
92. Vidal RL, Figueroa A, Court FA, Thielen P, Molina C, Wirth C, Caballero B, Kiffin R, Segura-Aguilar J, Cuervo AM, Glimcher LH, Hetz C, (2012) Targeting the UPR transcription factor XBP1 protects against Huntington's disease through the regulation of FoxO1 and autophagy. Hum Mol Genet 21: 2245-2262
93. Vogt G, Vogt B, Chuzhanova N, Julenius K, Cooper DN, Casanova JL, (2007) Gain-of-glycosylation mutations. Curr Opin Genet Dev 17: 245-251
94. Walker AK, Farg MA, Bye CR, McLean CA, Horne MK, Atkin JD, (2010) Protein disulphide isomerase protects against protein aggregation and is S-nitrosylated in amyotrophic lateral sclerosis. Brain 133: 105-116
95. Walter P, Ron D, (2011) The unfolded protein response: from stress pathway to homeostatic regulation. Science 334: 1081-1086
96. Wang M, Wen H, Brehm P, (2008) Function of neuromuscular synapses in the zebrafish choline-acetyltransferase mutant bajan. J Neurophysiol 100: 1995-2004
97. Wang C, Yu J, Huo L, Wang L, Feng W, Wang CC, (2012) Human protein-disulfide isomerase is a redox-regulated chaperone activated by oxidation of domain a'. J Biol Chem 287: 1139-1149
98. Yang Q, Guo ZB, (2015) Polymorphisms in protein disulfide isomerase are associated with sporadic amyotrophic lateral sclerosis in the Chinese Han population. Int J Neurosci 18: 1-19
99. Zhao L, Longo-Guess C, Harris BS, Lee JW, Ackerman SL, (2005) Protein accumulation and neurodegeneration in the woozy mutant mouse is caused by disruption of SIL1, a cochaperone of BiP. Nat Genet 37: 974-979