How lamina-associated polypeptide 1 (LAP1) activates Torsin

eLife

Volumn 3, Issue August2014, 2014, Pages 1-13

  Sosa, Brian A ^a   Esra Demircioglu, F ^a   Chen, James Z ^a   Ingram, Jessica ^a,b   Ploegh, Hidde L ^a,b   Schwartz, Thomas U ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ARGININE; CHAPERONE; LAP1B PROTEIN, HUMAN; MEMBRANE PROTEIN; NUCLEAR PROTEIN; PROTEIN BINDING; TOR1A PROTEIN, HUMAN;

AMINO ACID SEQUENCE; BINDING SITE; CELL NUCLEUS MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; DYSTONIC DISORDER; ELECTRON MICROSCOPY; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; MUTATION; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; X RAY CRYSTALLOGRAPHY;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; ARGININE; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DYSTONIC DISORDERS; HUMANS; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON; MODELS, MOLECULAR; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR ENVELOPE; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84909618559     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.03239     Document Type: Article

References (38)

1. Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallographica Section D, Biological Crystallography 66:213-221. doi: 10.1107/S0907444909052925.
2. Andersen KR, Leksa NC, Schwartz TU. 2013. Optimized E. coli expression strain LOBSTR eliminates common contaminants from His-tag purification. Proteins 81:1857-1861. doi: 10.1002/prot.24364.
3. Biegert A, Mayer C, Remmert M, Söding J, Lupas AN. 2006. The MPI Bioinformatics Toolkit for protein sequence analysis. Nucleic Acids Research 34:W335-W339. doi: 10.1093/nar/gkl217.
4. Breakefield XO, Blood AJ, Li Y, Hallett M, Hanson PI, Standaert DG. 2008. The pathophysiological basis of dystonias. Nature Reviews Neuroscience 9:222-234. doi: 10.1038/nrn2337.
5. Chen VB, Arendall WB, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. 2010. MolProbity: all-atom structure validation for macrmolecular crystallography. Acta Crystallographica Section D, Biological Crystallography 66:12-21. doi: 10.1107/S0907444909042073.
6. Edgar RC. 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113. doi: 10.1186/1471-2105-5-113.
7. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallographica Section D, Biological Crystallography 66:486-501. doi: 10.1107/S0907444910007493.
8. Erzberger JP, Berger JM. 2006. Evolutionary relationships and structural mechanisms of AAA+ proteins. Annual Review of Biophysics and Biomolecular Structure 35:93-114. doi: 10.1146/annurev.biophys.35.040405.101933.
9. Goodchild RE, Dauer WT. 2005. The AAA+ protein torsinA interacts with a conserved domain present in LAP1 and a novel ER protein. The Journal of Cell Biology 168:855-862. doi: 10.1083/jcb.200411026.
10. Granata A, Warner TT. 2010. The role of torsinA in dystonia. European Journal of Neurology 17(suppl 1):81-87. doi: 10.1111/j.1468-1331.2010.03057.x.
11. Gribun A, Cheung KL, Huen J, Ortega J, Houry WA. 2008. Yeast Rvb1 and Rvb2 are ATP-dependent DNA helicases that form a heterohexameric complex. Journal of Molecular Biology 376:1320-1333. doi: 10.1016/j.jmb.2007.12.049.
12. Hanson PI, Whiteheart SW. 2005. AAA+ proteins: have engine, will work. Nature Reviews Molecular Cell Biology 6:519-529. doi: 10.1038/nrm1684.
13. Hill CP, Babst M. 2012. Structure and function of the membrane deformation AAA ATPase Vps4. Biochimica et Biophysica Acta 1823:172-181. doi: 10.1016/j.bbamcr.2011.08.017.
14. Iyer LM, Leipe DD, Koonin EV, Aravind L. 2004. Evolutionary history and higher order classification of AAA+ ATPases. Journal of Structural Biology 146:11-31. doi: 10.1016/j.jsb.2003.10.010.
15. Jokhi V, Ashley J, Nunnari J, Noma A, Ito N, Wakabayashi-Ito N, Moore MJ, Budnik V. 2013. Torsin mediates primary envelopment of large ribonucleoprotein granules at the nuclear envelope. Cell Reports 3:988-995. doi: 10.1016/j.celrep.2013.03.015.
16. Kelley LA, Sternberg MJ. 2009. Protein structure prediction on the Web: a case study using the Phyre server. Nature Protocols 4:363-371. doi: 10.1038/nprot.2009.2.
17. Kock N, Naismith TV, Boston HE, Ozelius LJ, Corey DP, Breakefield XO, Hanson PI. 2006. Effects of genetic variations in the dystonia protein torsinA: identification of polymorphism at residue 216 as protein modifier. Human Molecular Genetics 15:1355-1364. doi: 10.1093/hmg/ddl055.
18. Maass DR, Sepulveda J, Pernthaner A, Shoemaker CB. 2007. Alpaca (Lama pacos) as a convenient source of recombinant camelid heavy chain antibodies (VHHs). Journal of Immunological Methods 324:13-25. doi: 10.1016/j.jim.2007.04.008.
19. McCullough J, Colf LA, Sundquist WI. 2013. Membrane fission reactions of the mammalian ESCRT pathway. Annual Review of Biochemistry 82:663-692. doi: 10.1146/annurev-biochem-072909-101058.
20. Morin A, Eisenbraun B, Key J, Sanschagrin PC, Timony MA, Ottaviano M, Sliz P. 2013. Collaboration gets the most out of software. eLife 2:e01456. doi: 10.7554/eLife.01456.
21. Naismith TV, Dalal S, Hanson PI. 2009. Interaction of torsinA with its major binding partners is impaired by the dystonia-associated Delta GAG deletion. The Journal of Biological Chemistry 284:27866-27874. doi: 10.1074/jbc.M109.020164.
22. Norby JG. 1988. Coupled assay of Na,K-ATPase activity. Methods in Enzymology 156:116-119. doi: 10.1016/0076-6879(88)56014-7.
23. Otwinowski Z, Minor W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods in Enzymology 276:307-326. doi: 10.1016/S0076-6879(97)76066-X.
24. Ozelius LJ, Hewett JW, Page CE, Bressman SB, Kramer PL, Shalish C, de Leon D, Brin MF, Raymond D, Corey DP, Fahn S, Risch NJ, Buckler AJ, Gusella JF, Breakefield XO. 1997. The early-onset torsion dystonia gene (DYT1) encodes an ATP-binding protein. Nature Genetics 17:40-48. doi: 10.1038/ng0997-40.
25. Rose A, Schlieker C. 2012. Alternative nuclear transport for cellular protein quality control. Trends in Cell Biology 22:509-514. doi: 10.1016/j.tcb.2012.07.003.
26. Saffian D, Grimm I, Girzalsky W, Erdmann R. 2012. ATP-dependent assembly of the heteromeric Pex1p-Pex6p-complex of the peroxisomal matrix protein import machinery. Journal of Structural Biology 179:126-132. doi: 10.1016/j.jsb.2012.06.002.
27. Senior A, Gerace L. 1988. Integral membrane proteins specific to the inner nuclear membrane and associated with the nuclear lamina. The Journal of Cell Biology 107:2029-2036. doi: 10.1083/jcb.107.6.2029.
28. Speese SD, Ashley J, Jokhi V, Nunnari J, Barria R, Li Y, Ataman B, Koon A, Chang Y-T, Li Q, Moore MJ, Budnik V. 2012. Nuclear envelope budding enables large ribonucleoprotein particle export during synaptic Wnt signaling. Cell 149:832-846. doi: 10.1016/j.cell.2012.03.032.
29. Vander Heyden AB, Naismith TV, Snapp EL, Hanson PI. 2011. Static retention of the lumenal monotopic membrane protein torsinA in the endoplasmic reticulum. The EMBO Journal 30:3217-3231. doi: 10.1038/emboj.2011.233.
30. Vander Heyden AB, Naismith TV, Snapp EL, Hodzic D, Hanson PI. 2009. LULL1 retargets TorsinA to the nuclear envelope revealing an activity that is impaired by the DYT1 dystonia mutation. Molecular Biology of the Cell 20:2661-2672. doi: 10.1091/mbc.E09-01-0094.
31. Wang F, Mei Z, Qi Y, Yan C, Hu Q, Wang J, Shi Y. 2011. Structure and mechanism of the hexameric MecA-ClpC molecular machine. Nature 471:331-335. doi: 10.1038/nature09780.
32. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ. 2009. Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189-1191. doi: 10.1093/bioinformatics/btp033.
33. Wendler P, Ciniawsky S, Kock M, Kube S. 2012. Structure and function of the AAA+ nucleotide binding pocket. Biochimica et Biophysica Acta 1823:2-14. doi: 10.1016/j.bbamcr.2011.06.014.
34. Xia D, Esser L, Singh SK, Guo F, Maurizi MR. 2004. Crystallographic investigation of peptide binding sites in the N-domain of the ClpA chaperone. Journal of Structural Biology 146:166-179. doi: 10.1016/j.jsb.2003.11.025.
35. Zeymer C, Barends TR, Werbeck ND, Schlichting I, Reinstein J. 2014. Elements in nucleotide sensing and hydrolysis of the AAA+ disaggregation machine ClpB: a structure-based mechanistic dissection of a molecular motor. Acta Crystallographica Section D, Biological Crystallography 70:582-595. doi: 10.1107/S1399004713030629.
36. Zhao C, Brown RS, Chase AR, Eisele MR, Schlieker C. 2013. Regulation of Torsin ATPases by LAP1 and LULL1. Proceedings of the National Academy of Sciences of USA 110:E1545-E1554. doi: 10.1073/pnas.1300676110.
37. Zhu L, Mendoza JL, Thomas PJ. 2010. A unique redox-sensing sensor II motif in TorsinA plays a critical role in nucleotide and partner binding. Journal of Biological Chemistry 285:37271-37280. doi: 10.1074/jbc.M110.123471.
38. Zhu L, Wrabl JO, Hayashi AP, Rose LS, Thomas PJ. 2008. The torsin-family AAA+ protein OOC-5 contains a critical disulfide adjacent to Sensor-II that couples redox state to nucleotide binding. Molecular Biology of the Cell 19:3599-3612. doi: 10.1091/mbc.E08-01-0015.