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Critical Reviews in Biochemistry and Molecular Biology Volume 50, 2015 - Issue 6
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Review Article

Torsins: not your typical AAA+ ATPases

April E. RoseDepartment of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT, USA and
,
Rebecca S. H. BrownDepartment of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT, USA and
&
Christian SchliekerDepartment of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT, USA and ;Department of Cell Biology, Yale School of Medicine, New Haven, CT, USACorrespondence[email protected]
Pages 532-549 | Received 10 Aug 2015, Accepted 04 Sep 2015, Published online: 13 Oct 2015

References

  • Augustin S, Gerdes F, Lee S, et al. (2009). An intersubunit signaling network coordinates ATP hydrolysis by m-AAA proteases. Mol Cell 35:574–85
  • Babst M, Wendland B, Estepa EJ, Emr SD. (1998). The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function. EMBO J 17:2982–93
  • Basham SE, Rose LS. (1999). Mutations in ooc-5 and ooc-3 disrupt oocyte formation and the reestablishment of asymmetric PAR protein localization in two-cell Caenorhabditis elegans embryos. Dev Biol 215:253–63
  • Basham SE, Rose LS. (2001). The Caenorhabditis elegans polarity gene ooc-5 encodes a Torsin-related protein of the AAA ATPase superfamily. Development 128:4645–56
  • Bhabha G, Cheng HC, Zhang N, et al. (2014). Allosteric communication in the dynein motor domain. Cell 159:857–68
  • Bowman GD, O'Donnell M, Kuriyan J. (2004). Structural analysis of a eukaryotic sliding DNA clamp-clamp loader complex. Nature 429:724–30
  • Bragg DC, Camp SM, Kaufman CA, et al. (2004a). Perinuclear biogenesis of mutant torsin-A inclusions in cultured cells infected with tetracycline-regulated herpes simplex virus type 1 amplicon vectors. Neuroscience 125:651–61
  • Bragg DC, Kaufman CA, Kock N, Breakefield XO. (2004b). Inhibition of N-linked glycosylation prevents inclusion formation by the dystonia-related mutant form of torsinA. Mol Cell Neurosci 27:417–26
  • Bressman SB, De Leon D, Brin MF, et al. (1989). Idiopathic dystonia among Ashkenazi Jews: evidence for autosomal dominant inheritance. Ann Neurol 26:612–20
  • Bressman SB, De Leon D, Kramer PL, et al. (1994). Dystonia in Ashkenazi Jews: clinical characterization of a founder mutation. Ann Neurol 36:771–7
  • Brown RS, Zhao C, Chase AR, et al. (2014). The mechanism of Torsin ATPase activation. Proc Natl Acad Sci USA 111:E4822–31
  • Buchsbaum S, Bercovich B, Ziv T, Ciechanover A. (2012). Modification of the inflammatory mediator LRRFIP2 by the ubiquitin-like protein FAT10 inhibits its activity during cellular response to LPS. Biochem Biophys Res Commun 428:11–16
  • Buck TM, Plavchak L, Roy A, et al. (2013). The Lhs1/GRP170 chaperones facilitate the endoplasmic reticulum-associated degradation of the epithelial sodium channel. J Biol Chem 288:18366–80
  • Burdette AJ, Churchill PF, Caldwell GA, Caldwell KA. (2010). The early-onset torsion dystonia-associated protein, torsinA, displays molecular chaperone activity in vitro. Cell Stress Chaperones 15:605–17
  • Burton RE, Siddiqui SM, Kim YI, et al. (2001). Effects of protein stability and structure on substrate processing by the ClpXP unfolding and degradation machine. EMBO J 20:3092–100
  • Calakos N, Patel VD, Gottron M, et al. (2010). Functional evidence implicating a novel TOR1A mutation in idiopathic, late-onset focal dystonia. J Med Genet 47:646–50
  • Caldwell GA, Cao S, Sexton EG, et al. (2003). Suppression of polyglutamine-induced protein aggregation in Caenorhabditis elegans by torsin proteins. Hum Mol Genet 12:307–19
  • Cashikar AG, Schirmer EC, Hattendorf DA, et al. (2002). Defining a pathway of communication from the C-terminal peptide binding domain to the N-terminal ATPase domain in a AAA protein. Mol Cell 9:751–60
  • Chen P, Burdette AJ, Porter JC, et al. (2010a). The early-onset torsion dystonia-associated protein, torsinA, is a homeostatic regulator of endoplasmic reticulum stress response. Hum Mol Genet 19:3502–15
  • Chen XP, Hu XH, Wu SH, et al. (2010b). RNA interference-mediated inhibition of wild-type Torsin A expression increases apoptosis caused by oxidative stress in cultured cells. Neurochem Res 35:1214–23
  • Cheng FB, Feng JC, Ma LY, et al. (2014). Combined occurrence of a novel TOR1A and a THAP1 mutation in primary dystonia. Mov Disord 29:1079–83
  • Cho C, Vale RD. (2012). The mechanism of dynein motility: insight from crystal structures of the motor domain. Biochim Biophys Acta 1823:182–91
  • Crisp M, Liu Q, Roux K, et al. (2006). Coupling of the nucleus and cytoplasm: role of the LINC complex. J Cell Biol 172:41–53
  • Dalal S, Rosser MF, Cyr DM, Hanson PI. (2004). Distinct roles for the AAA ATPases NSF and p97 in the secretory pathway. Mol Biol Cell 15:637–48
  • Davies JM, Brunger AT, Weis WI. (2008). Improved structures of full-length p97, an AAA ATPase: implications for mechanisms of nucleotide-dependent conformational change. Structure 16:715–26
  • Dephoure N, Zhou C, Villen J, et al. (2008). A quantitative atlas of mitotic phosphorylation. Proc Natl Acad Sci USA 105:10762–67
  • Dorboz I, Coutelier M, Bertrand AT, et al. (2014). Severe dystonia, cerebellar atrophy, and cardiomyopathy likely caused by a missense mutation in TOR1AIP1. Orphanet J Rare Dis 9:174
  • Dron M, Meritet JF, Dandoy-Dron F, et al. (2002). Molecular cloning of ADIR, a novel interferon responsive gene encoding a protein related to the torsins. Genomics 79:315–25
  • Edgar RC. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res, 32:1792–7
  • Erzberger JP, Berger JM. (2006). Evolutionary relationships and structural mechanisms of AAA+ proteins. Annu Rev Biophys Biomol Struct 35:93–114
  • Foisner R, Gerace L. (1993). Integral membrane proteins of the nuclear envelope interact with lamins and chromosomes, and binding is modulated by mitotic phosphorylation. Cell 73:1267–79
  • Glynn SE, Martin A, Nager AR, et al. (2009). Structures of asymmetric ClpX hexamers reveal nucleotide-dependent motions in a AAA+ protein-unfolding machine. Cell 139:744–56
  • Gonzalez-Alegre P, Paulson HL. (2004). Aberrant cellular behavior of mutant torsinA implicates nuclear envelope dysfunction in DYT1 dystonia. J Neurosci 24:2593–601
  • Goodchild RE, Buchwalter AL, Naismith TV, et al. (2015). Access of torsinA to the inner nuclear membrane is activity dependent and regulated in the endoplasmic reticulum. J Cell Sci 128:2854–65
  • Goodchild RE, Dauer WT. (2004). Mislocalization to the nuclear envelope: an effect of the dystonia-causing torsinA mutation. Proc Natl Acad Sci USA, 101:847–52
  • Goodchild RE, Dauer WT. (2005). The AAA+ protein torsinA interacts with a conserved domain present in LAP1 and a novel ER protein. J Cell Biol 168:855–62
  • Goodchild RE, Kim CE, Dauer WT. (2005). Loss of the dystonia-associated protein torsinA selectively disrupts the neuronal nuclear envelope. Neuron 48:923–32
  • Granata A, Koo SJ, Haucke V, et al. (2011). CSN complex controls the stability of selected synaptic proteins via a torsinA-dependent process. EMBO J, 30:181–93
  • Granata A, Watson R, Collinson LM, et al. (2008). The dystonia-associated protein torsinA modulates synaptic vesicle recycling. J Biol Chem 283:7568–79
  • Guenther B, Onrust R, Sali A, et al. (1997). Crystal structure of the delta' subunit of the clamp-loader complex of E. coli DNA polymerase III. Cell 91:335–45
  • Hanson PI, Whiteheart SW. (2005). AAA+ proteins: have engine, will work. Nat Rev Mol Cell Biol 6:519–29
  • Hedglin M, Kumar R, Benkovic SJ. (2013). Replication clamps and clamp loaders. Cold Spring Harb Perspect Biol 5:a010165
  • Helaers R, Milinkovitch MC. (2010). MetaPIGA v2.0: maximum likelihood large phylogeny estimation using the metapopulation genetic algorithm and other stochastic heuristics. BMC Bioinformatics 11:379
  • Hewett J, Gonzalez-Agosti C, Slater D, et al. (2000). Mutant torsinA, responsible for early-onset torsion dystonia, forms membrane inclusions in cultured neural cells. Hum Mol Genet 9:1403–13
  • Hewett J, Ziefer P, Bergeron D, et al. (2003). TorsinA in PC12 cells: localization in the endoplasmic reticulum and response to stress. J Neurosci Res 72:158–68
  • Hewett JW, Kamm C, Boston H, et al. (2004). TorsinB-perinuclear location and association with torsinA. . J Neurochem 89:1186–94
  • Hewett JW, Nery FC, Niland B, et al. (2008). siRNA knock-down of mutant torsinA restores processing through secretory pathway in DYT1 dystonia cells. Hum Mol Genet 17:1436–45
  • Hewett JW, Tannous B, Niland BP, et al. (2007). Mutant torsinA interferes with protein processing through the secretory pathway in DYT1 dystonia cells. Proc Natl Acad Sci USA 104:7271–6
  • Hewett JW, Zeng J, Niland BP, et al. (2006). Dystonia-causing mutant torsinA inhibits cell adhesion and neurite extension through interference with cytoskeletal dynamics. Neurobiol Dis 22:98–111
  • Hu J, Prinz WA, Rapoport TA. (2011). Weaving the web of ER tubules. Cell 147:1226–31
  • Jeruzalmi D, O'Donnell M, Kuriyan J. (2001). Crystal structure of the processivity clamp loader gamma (gamma) complex of E. coli DNA polymerase III. Cell 106:429–41
  • Johnson A, O'Donnell M. (2003). Ordered ATP hydrolysis in the gamma complex clamp loader AAA+ machine. J Biol Chem 278:14406–13
  • Jokhi V, Ashley J, Ninnari J, et al. (2013). Torsin mediates primary envelopment of large ribonucleoprotein granules at the nuclear envelope. Cell Rep 3:988–95
  • Jungwirth M, Dear ML, Brown P, et al. (2010). Relative tissue expression of homologous torsinB correlates with the neuronal specific importance of DYT1 dystonia-associated torsinA. Hum Mol Genet 19:888–900
  • Kakazu Y, Koh JY, Ho KW, et al. (2012a). Synaptic vesicle recycling is enhanced by torsinA that harbors the DYT1 dystonia mutation. Synapse 66:453–64
  • Kakazu Y, Koh JY, Iwabuchi S, et al. (2012b). Miniature release events of glutamate from hippocampal neurons are influenced by the dystonia-associated protein torsinA. Synapse 66:807–22
  • Kamm C, Boston H, Hewett J, et al. (2004). The early onset dystonia protein torsinA interacts with kinesin light chain 1. J Biol Chem 279:19882–92
  • Karlberg T, Van Denberg S, Hammarstorm M, et al. (2009). Crystal structure of the ATPase domain of the human AAA+ protein paraplegin/SPG7. PLoS One 4:e6975
  • Kato JY, Yoneda-Kato N. (2009). Mammalian COP9 signalosome. Genes Cells 14:1209–25
  • Kayman-Kurekci G, Talim B, Korkusuz P, et al. (2014). Mutation in TOR1AIP1 encoding LAP1B in a form of muscular dystrophy: a novel gene related to nuclear envelopathies. Neuromuscul Disord 24:624–33
  • Kim CE, Perez A, Perkins G, et al. (2010). A molecular mechanism underlying the neural-specific defect in torsinA mutant mice. Proc Natl Acad Sci USA 107:9861–6
  • Konakova M, Pulst SM. (2005). Dystonia-associated forms of torsinA are deficient in ATPase activity. J Mol Neurosci 25:105–17
  • Kustedjo K, Bracey MH, Cravatt BF. (2000). Torsin A and its torsion dystonia-associated mutant forms are lumenal glycoproteins that exhibit distinct subcellular localizations. J Biol Chem 275:27933–39
  • Kustedjo K, Deechongkit S, Kelly JW, Cravatt BF. (2003). Recombinant expression, purification, and comparative characterization of torsinA and its torsion dystonia-associated variant Delta E-torsinA. Biochemistry 42:15333–41
  • Lee S, Sowa ME, Watanabe YH, et al. (2003). The structure of ClpB: a molecular chaperone that rescues proteins from an aggregated state. Cell 115:229–40
  • Lenzen CU, Steinmann D, Whiteheart SW, Weis WI. (1998). Crystal structure of the hexamerization domain of N-ethylmaleimide-sensitive fusion protein. Cell 94:525–36
  • Leung JC, Klein C, Friedman J, et al. (2001). Novel mutation in the TOR1A (DYT1) gene in atypical early onset dystonia and polymorphisms in dystonia and early onset parkinsonism. Neurogenetics 3:133–43
  • Li H, Wu HC, Liu Z, et al. (2014). Intracellular complexes of the early-onset torsion dystonia-associated AAA+ ATPase TorsinA. Springerplus 3:743
  • Liang CC, Tanabe LM, Jou S, et al. (2014). TorsinA hypofunction causes abnormal twisting movements and sensorimotor circuit neurodegeneration. J Clin Invest 124:3080–92
  • Marchler-Bauer A, Lu S, Anderson JB, et al. (2011). CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res 39:D225–29
  • Maric M, Shao J, Ryan RJ, et al. (2011). A functional role for TorsinA in herpes simplex virus 1 nuclear egress. J Virol 85:9667–79
  • McCullough J, Colf LA, Sundquist WI. (2013). Membrane fission reactions of the mammalian ESCRT pathway. Annu Rev Biochem 82:663–92
  • McCullough J, Sundquist WI. (2014). Putting a finger in the ring. Nat Struct Mol Biol 21:1025–27
  • Mclean PJ, Kawamata H, Shariff S, et al. (2002). TorsinA and heat shock proteins act as molecular chaperones: suppression of alpha-synuclein aggregation. J Neurochem 83:846–54
  • Mettenleiter TC, Klupp BG, Granzow H. (2009). Herpesvirus assembly: an update. Virus Res 143:222–34
  • Meyer H, Bug M, Bremer S. (2012). Emerging functions of the VCP/p97 AAA-ATPase in the ubiquitin system. Nat Cell Biol 14:117–23
  • Mogk A, Schlieker C, Strub C, et al. (2003). Roles of individual domains and conserved motifs of the AAA+ chaperone ClpB in oligomerization, ATP hydrolysis, and chaperone activity. J Biol Chem 278:17615–24
  • Nagy M, Wu HC, Liu Z, et al. (2009). Walker-A threonine couples nucleotide occupancy with the chaperone activity of the AAA+ ATPase ClpB. Protein Sci 18:287–93
  • Naismith TV, Dalal S, Hanson PI. (2009). Interaction of torsinA with its major binding partners is impaired by the dystonia-associated DeltaGAG deletion. J Biol Chem 284:27866–74
  • Nery FC, Armata IA, Farley JE, et al. (2011). TorsinA participates in endoplasmic reticulum-associated degradation. Nat Commun 2:393
  • Nery FC, Zeng J, Niland BP, et al. (2008). TorsinA binds the KASH domain of nesprins and participates in linkage between nuclear envelope and cytoskeleton. J Cell Sci 121:3476–86
  • Neumann B, Walter T, Heriche JK, et al. (2010). Phenotypic profiling of the human genome by time-lapse microscopy reveals cell division genes. Nature 464:721–7
  • Neuwald AF, Aravind L, Spouge JL, Koonin EV. (1999). AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res 9:27–43
  • O'Donnell M, Kuriyan J. (2006). Clamp loaders and replication initiation. Curr Opin Struct Biol, 16:35–41
  • O'Farrell C, Lockhart PJ, Lincoln S, et al. (2004). Biochemical characterization of torsinB. Brain Res Mol Brain Res 127:1–9
  • Ogura T, Whiteheart SW, Wilikinson AJ. (2004). Conserved arginine residues implicated in ATP hydrolysis, nucleotide-sensing, and inter-subunit interactions in AAA and AAA+ ATPases. J Struct Biol 146:106–12
  • Olmos Y, Hodgson L, Mantell J, et al. (2015). ESCRT-III controls nuclear envelope reformation. Nature 522:236–9
  • Osborne AR, Rapoport TA, Van den Berg B. (2005). Protein translocation by the Sec61/SecY channel. Annu Rev Cell Dev Biol 21:529–50
  • Ozelius LJ, Hewett JW, Page CE, et al. (1997). The early-onset torsion dystonia gene (DYT1) encodes an ATP-binding protein. Nat Genet 17:40–8
  • Ozelius LJ, Hewett JW, Page CE, et al. (1998). The gene (DYT1) for early-onset torsion dystonia encodes a novel protein related to the Clp protease/heat shock family. Adv Neurol 78:93–105
  • Ozelius LJ, Page CE, Klein C, et al. (1999). The TOR1A (DYT1) gene family and its role in early onset torsion dystonia. Genomics 62:377–84
  • Pappas SS, Darr K, Holley SM, et al. (2015). Forebrain deletion of the dystonia protein torsinA causes dystonic-like movements and loss of striatal cholinergic neurons. Elife 4:e08352
  • Pham P, Frei KP, Woo W, Truong DD. (2006). Molecular defects of the dystonia-causing torsinA mutation. Neuroreport 17:1725–8
  • Rose A, Schlieker C. (2012). Alternative nuclear transport for cellular protein quality control. Trends Cell Biol 22:509–14
  • Rose AE, Zhao C, Turner EM, et al. (2014). Arresting a Torsin ATPase reshapes the endoplasmic reticulum. J Biol Chem 289:552–64
  • Santos M, Domingues SC, Costa P, et al. (2014). Identification of a novel human LAP1 isoform that is regulated by protein phosphorylation. PLoS One 9:e113732
  • Saraste M, Sibbald PR, Wittinghofer A. (1990). The P-loop-a common motif in ATP- and GTP-binding proteins. Trends Biochem Sci 15:430–4
  • Sauer RT, Baker TA. (2011). AAA+ proteases: ATP-fueled machines of protein destruction. Annu Rev Biochem 80:587–612
  • Scheffzek K, Ahamadian MR, Wittinghofer A. (1998). GTPase-activating proteins: helping hands to complement an active site. Trends Biochem Sci 23:257–62
  • Schlieker C, Weibezahn J, Patzelt H, et al. (2004). Substrate recognition by the AAA+ chaperone ClpB. Nat Struct Mol Biol 11:607–15
  • Senior A, Gerace L. (1988). Integral membrane proteins specific to the inner nuclear membrane and associated with the nuclear lamina. J Cell Biol 107:2029–36
  • Shin JY, Mendez-Lopez I, Wang Y, et al. (2013). Lamina-associated polypeptide-1 interacts with the muscular dystrophy protein emerin and is essential for skeletal muscle maintenance. Dev Cell 26:591–603
  • Siddiqui SM, Sauer RT, Baker TA. (2004). Role of the processing pore of the ClpX AAA+ ATPase in the recognition and engagement of specific protein substrates. Genes Dev 18:369–74
  • Simmen FA, Su Y, Xiao R, et al. (2008). The Krüppel-like factor 9 (KLF9) network in HEC-1-A endometrial carcinoma cells suggests the carcinogenic potential of dys-regulated KLF9 expression. Reprod Biol Endocrinol 6:41
  • Smith GR, Contreras-Moreira B, Zhang X, Bates PA. (2004). A link between sequence conservation and domain motion within the AAA+ family. J Struct Biol 146:189–204
  • Söding J, Biegert A, Lupas AN. (2005). The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33:W244–48
  • Sosa BA, Demircioglu FE, Chen JZ, et al. (2014). How lamina-associated polypeptide 1 (LAP1) activates Torsin. Elife 3:e03239
  • Speese SD, Ashley J, Jokhi V, et al. (2012). Nuclear envelope budding enables large ribonucleoprotein particle export during synaptic wnt signaling. Cell 149:832–46
  • Story RM, Weber IT, Steitz TA. (1992). The structure of the E. coli recA protein monomer and polymer. Nature 355:318–25
  • Sudhof TC, Rothman JE. (2009). Membrane fusion: grappling with SNARE and SM proteins. Science 323:474–7
  • Tanabe LM, Kim CE, Alagem N, Dauer WT. (2009). Primary dystonia: molecules and mechanisms. Nat Rev Neurol 5:598–609
  • Torres GE, Sweeney AL, Beaulieu JM, et al. (2004). Effect of torsinA on membrane proteins reveals a loss of function and a dominant-negative phenotype of the dystonia-associated DeltaE-torsinA mutant. Proc Natl Acad Sci U S A 101:15650–5
  • Turner EM, Brown RS, Laudermilch E, et al. (2015). The Torsin activator LULL1 is required for efficient growth of HSV-1. J Virol 89:8444–52
  • Vander Heyden AB, Naismith TV, Snapp EL, Hanson PI. (2011). Static retention of the lumenal monotopic membrane protein torsinA in the endoplasmic reticulum. EMBO J 30:3217–31
  • Vander Heyden AB, Naismith TV, Snapp EL, et al. (2009). LULL1 retargets TorsinA to the nuclear envelope revealing an activity that is impaired by the DYT1 dystonia mutation. Mol Biol Cell 20:2661–72
  • VanGompel MJ, Nguyen KC, Hall DH, et al. (2015). A novel function for the Caenorhabditis elegans torsin OOC-5 in nucleoporin localization and nuclear import. Mol Biol Cell 26:1752–63
  • Vasudevan A, Breakefield XO, Bhide PG. (2006). Developmental patterns of torsinA and torsinB expression. Brain Res 1073–1074:139–45
  • Vietri M, Schink KO, Campsteijn C, et al. (2015). Spastin and ESCRT-III coordinate mitotic spindle disassembly and nuclear envelope sealing. Nature 522:231–5
  • Vulinovic F, Lohmann K, Rakovic A, et al. (2014). Unraveling cellular phenotypes of novel TorsinA/TOR1A mutations. Hum Mutat 35:1114–22
  • Walter P, Ron D. (2011). The unfolded protein response: from stress pathway to homeostatic regulation. Science 334:1081–86
  • Wang WL, Lee YC, Yang WM, et al. (2008). Sumoylation of LAP1 is involved in the HDAC4-mediated repression of COX-2 transcription. Nucleic Acids Res 36:6066–79
  • Weber-Ban EU, Reid BG, Miranker AD, Horwich AL. (1999). Global unfolding of a substrate protein by the Hsp100 chaperone ClpA. Nature 401:90–3
  • Webster BM, Colombi P, Jager J, Lusk CP. (2014). Surveillance of nuclear pore complex assembly by ESCRT-III/Vps4. Cell 159:388–401
  • Weibezahn J, Schlieker C, Bukau B, Mogk A. (2003). Characterization of a trap mutant of the AAA+ chaperone ClpB. J Biol Chem 278:32608–17
  • Weibezahn J, Tessarz P, Schlieker C, et al. (2004). Thermotolerance requires refolding of aggregated proteins by substrate translocation through the central pore of ClpB. Cell 119:653–65
  • Whiteheart SW, Rossnagel K, Buhrow SA, et al. (1994). N-ethylmaleimide-sensitive fusion protein: a trimeric ATPase whose hydrolysis of ATP is required for membrane fusion. J Cell Biol 126:945–54
  • Yamada-Inagawa T, Okuno T, Karata K, et al. (2003). Conserved pore residues in the AAA protease FtsH are important for proteolysis and its coupling to ATP hydrolysis. J Biol Chem 278:50182–87
  • Yu RC, Hanson PI, Jahn R, Brunger AT. (1998). Structure of the ATP-dependent oligomerization domain of N-ethylmaleimide sensitive factor complexed with ATP. Nat Struct Biol 5:803–11
  • Zacchi LF, Wu HC, Bell SL, et al. (2014). The BiP molecular chaperone plays multiple roles during the biogenesis of torsinA, an AAA+ ATPase associated with the neurological disease early-onset torsion dystonia. J Biol Chem 289:12727–47
  • Zhang X, Shaw A, Bates PA, et al. (2000). Structure of the AAA ATPase p97. Mol Cell, 6:1473–84
  • Zhao C, Brown RS, Chase AR, et al. (2013). Regulation of Torsin ATPases by LAP1 and LULL1. Proc Natl Acad Sci USA, 110:E1545–54
  • Zhao M, Wu S, Zhou Q, et al. (2015). Mechanistic insights into the recycling machine of the SNARE complex. Nature 518:61–7
  • Zhu L, Millen L, Mendoza JL, Thomas PJ. (2010). A unique redox-sensing sensor II motif in TorsinA plays a critical role in nucleotide and partner binding. J Biol Chem 285:37271–80
  • Zhu L, Wrabl JO, Hayashi AP, et al. (2008). The torsin-family AAA+ protein OOC-5 contains a critical disulfide adjacent to Sensor-II that couples redox state to nucleotide binding. Mol Biol Cell 19:3599–612
  • Zirn B, Grundmann K, Huppke P, et al. (2008). Novel TOR1A mutation p.Arg288Gln in early-onset dystonia (DYT1). J Neurol Neurosurg Psychiatry 79:1327–30

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