Arresting a Torsin ATPase reshapes the endoplasmic reticulum

Journal of Biological Chemistry

Volumn 289, Issue 1, 2014, Pages 552-564

  Rose, April E ^a   Zhao, Chenguang ^a   Turner, Elizabeth M ^a   Steyer, Anna M ^a   Schlieker, Christian ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGY;

AROMATIC MOTIFS; ATP-ASE ACTIVITY; ATPASES; C TERMINUS; ENDOPLASMIC RETICULUM; NUCLEAR ENVELOPE; SINUSOIDAL STRUCTURES;

CELL MEMBRANES;

MEMBRANE PROTEIN; PROTEIN LULL1; REGULATOR PROTEIN; TORSINB PROTEIN; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; CARRIER PROTEIN; CHAPERONE; TOR1AIP2 PROTEIN, HUMAN; TOR1B PROTEIN, HUMAN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL COMPARTMENTALIZATION; CELL EXPANSION; CELL NUCLEUS MEMBRANE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; MEMBRANE STRUCTURE; MOLECULAR DYNAMICS; MUTATION RATE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN MOTIF; ENZYMOLOGY; GENETICS; HELA CELL LINE; HUMAN; INTRACELLULAR MEMBRANE; METABOLISM; MUTATION;

ADENOSINE TRIPHOSPHATASES; AMINO ACID MOTIFS; CARRIER PROTEINS; ENDOPLASMIC RETICULUM; HELA CELLS; HUMANS; INTRACELLULAR MEMBRANES; MEMBRANE PROTEINS; MOLECULAR CHAPERONES; MUTATION;

EID: 84891672651     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.515791     Document Type: Article

References (40)

1. Neuwald, A. F., Aravind, L., Spouge, J. L., and Koonin, E. V. (1999) AAA+: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res. 9, 27-43 (Pubitemid 29095146)
2. Ozelius, L. J., Hewett, J. W., Page, C. E., Bressman, S. B., Kramer, P. L., Shalish, C., De Leon, D., Brin, M. F., Raymond, D., Corey, D. P., Fahn, S., Risch, N. J., Buckler, A. J., Gusella, J. F., and Breakefield, X. O. (1997) The early-onset torsion dystonia gene (DYT1) encodes an ATP-binding protein. Nat Genet. 17, 40-48 (Pubitemid 27377530)
3. Hewett, J., Gonzalez-Agosti, C., Slater, D., Ziefer, P., Li, S., Bergeron, D., Jacoby, D. J., Ozelius, L. J., Ramesh, V., and Breakefield, X. O. (2000) Mutant torsinA, responsible for early-onset torsion dystonia, forms membrane inclusions in cultured neural cells. Hum. Mol. Genet. 9, 1403-1413 (Pubitemid 30312489)
4. Gonzalez-Alegre, P., and Paulson, H. L. (2004) Aberrant cellular behavior of mutant torsinA implicates nuclear envelope dysfunction in DYT1 dystonia. J. Neurosci. 24, 2593-2601 (Pubitemid 38380935)
5. Goodchild, R. E., and Dauer, W. T. (2004) Mislocalization to the nuclear envelope: an effect of the dystonia-causing torsinA mutation. Proc. Natl. Acad. Sci. U. S. A. 101, 847-852 (Pubitemid 38121046)
6. Goodchild, R. E., Kim, C. E., and Dauer, W. T. (2005) Loss of the dystonia-associated protein torsinA selectively disrupts the neuronal nuclear envelope. Neuron 48, 923-932 (Pubitemid 41814697)
7. Naismith, T. V., Heuser, J. E., Breakefield, X. O., and Hanson, P. I. (2004) TorsinA in the nuclear envelope. Proc. Natl. Acad. Sci. U. S. A. 101, 7612-7617 (Pubitemid 38658077)
8. Naismith, T. V., Dalal, S., and Hanson, P. I. (2009) Interaction of torsinA with its major binding partners is impaired by the dystonia-associated DeltaGAG deletion. J. Biol. Chem. 284, 27866-27874
9. Zhao, C., Brown, R. S., Chase, A. R., Eisele, M. R., and Schlieker, C. (2013) Regulation of Torsin ATPases by LAP1 and LULL1. Proc. Natl. Acad. Sci. U. S. A. 110, E1545-E1554
10. Goodchild, R. E., and Dauer, W. T. (2005) The AAA+ protein torsinA interacts with a conserved domain present in LAP1 and a novel ER protein. J. Cell Biol. 168, 855-862 (Pubitemid 40397000)
11. Jungwirth, M., Dear, M. L., Brown, P., Holbrook, K., and Goodchild, R. (2010) Relative tissue expression of homologous torsinB correlates with the neuronal specific importance of DYT1 dystonia-associated torsinA. Hum. Mol. Genet. 19, 888-900
12. Jokhi, V., Ashley, J., Nunnari, J., Noma, A., Ito, N., Wakabayashi-Ito, N., Moore, M. J., and Budnik, V. (2013) Torsin mediates primary envelopment of large ribonucleoprotein granules at the nuclear envelope. Cell Reports 3, 988-995
13. Kim, C. E., Perez, A., Perkins, G., Ellisman, M. H, and Dauer, W. T. (2010) A molecular mechanism underlying the neural-specific defect in torsinA mutant mice. Proc. Natl. Acad. Sci. U. S A. 107, 9861-9866
14. Foisner, R., and Gerace, L. (1993) Integral membrane proteins of the nuclear envelope interact with lamins and chromosomes, and binding is modulated by mitotic phosphorylation. Cell 73, 1267-1279 (Pubitemid 23201142)
15. Vander Heyden, A. B., Naismith, T. V., Snapp, E. L., Hodzic, D., and Hanson, P. I. (2009) LULL1 retargets TorsinA to the nuclear envelope revealing an activity that is impaired by the DYT1 dystonia mutation. Mol. Biol. Cell 20, 2661-2672
16. Snapp, E. L., Hegde, R. S., Francolini, M., Lombardo, F., Colombo, S., Pedrazzini, E., Borgese, N, and Lippincott-Schwartz, J. (2003) Formation of stacked ER cisternae by low affinity protein interactions. J. Cell Biol. 163, 257-269 (Pubitemid 37363127)
17. Borgese, N., Francolini, M., and Snapp, E. (2006) Endoplasmic reticulum architecture: structures in flux. Curr. Opin. Cell Biol. 18, 358-364 (Pubitemid 44016057)
18. Hurley, J. H., and Hanson, P. I. (2010) Membrane budding and scission by the ESCRT machinery: it's all in the neck. Nature Reviews 11, 556-566
19. Ferguson, S. M., and De Camilli, P. (2012) Dynamin, a membrane-remodelling GTPase. Nature Reviews. Molecular Cell Biology 13, 75-88
20. Hanson, P. I., and Whiteheart, S. W. (2005) AAA+ proteins: have engine, will work. Nature Reviews. Molecular Cell Biology 6, 519-529 (Pubitemid 40943043)
21. Bragg, D. C., Camp, S. M., Kaufman, C. A., Wilbur, J. D., Boston, H., Schuback, D. E., Hanson, P. I., Sena-Esteves, M., and Breakefield, X. O. (2004) Perinuclear biogenesis of mutant torsin-A inclusions in cultured cells infected with tetracycline-regulated herpes simplex virus type 1 amplicon vectors. Neuroscience 125, 651-661 (Pubitemid 38510175)
22. Kustedjo, K., Bracey, M. H, and Cravatt, B. F. (2000) Torsin A and its torsion dystonia-associated mutant forms are lumenal glycoproteins that exhibit distinct subcellular localizations. J. Biol. Chem. 275, 27933-27939
23. Bragg, D. C., Kaufman, C. A., Kock, N, and Breakefield, X. O. (2004) Inhibition of N-linked glycosylation prevents inclusion formation by the dystonia-related mutant form of torsinA. Mol. Cell Neurosci. 27, 417-426 (Pubitemid 39539996)
24. Hewett, J. W., Kamm, C., Boston, H., Beauchamp, R., Naismith, T., Ozelius, L., Hanson, P. I., Breakefield, X. O., and Ramesh, V. (2004) TorsinB-perinuclear location and association with torsinA. J. Neurochem. 89, 1186-1194
25. Görlich, D., Prehn, S., Hartmann, E., Kalies, K. U., and Rapoport, T. A. (1992) A mammalian homolog of SEC61p and SECYp is associated with ribosomes and nascent polypeptides during translocation. Cell 71, 489-503
26. Munro, S., and Pelham, H. R. (1987) A C-terminal signal prevents secretion of luminal ER proteins. Cell 48, 899-907
27. Crisp, M., Liu, Q., Roux, K., Rattner, J. B., Shanahan, C., Burke, B., Stahl, P. D., and Hodzic, D. (2006) Couplingof the nucleus and cytoplasm: role of the LINC complex. J. Cell Biol. 172, 41-53 (Pubitemid 43042628)
28. Nery, F. C., Zeng, J., Niland, B. P., Hewett, J., Farley, J., Irimia, D., Li, Y., Wiche, G., Sonnenberg, A., and Breakefield, X. O. (2008) TorsinA binds the KASH domain of nesprins and participates in linkage between nuclear envelope and cytoskeleton. J. Cell Sci. 121, 3476-3486
29. Voeltz, G. K., and Prinz, W. A. (2007) Sheets, ribbons and tubules - how organelles get their shape. Nature Reviews. Molecular Cell Biology 8, 258-264
30. Jones, T. R., Wiertz, E. J., Sun, L., Fish, K. N., Nelson, J. A., and Ploegh, H. L. (1996) Human cytomegalovirus US3 impairs transport and maturation of major histocompatibility complex class I heavy chains. Proc. Natl. Acad. Sci. U. S. A. 93, 11327-11333 (Pubitemid 26347121)
31. Zhao, G., Zhou, X., Wang, L., Li, G., Schindelin, H., and Lennarz, W. J. (2007) Studies on peptide: N-glycanase-p97 interaction suggest that p97 phosphorylation modulates endoplasmic reticulum-associated degradation. Proc. Natl. Acad. Sci. U. S. A. 104, 8785-8790 (Pubitemid 47175389)
32. Smith, D. M., Fraga, H., Reis, C., Kafri, G., and Goldberg, A. L. (2011) ATP binds to proteasomal ATPases in pairs with distinct functional effects, implying an ordered reaction cycle. Cell 144, 526-538
33. Shibata, Y., Hu, J., Kozlov, M. M., and Rapoport, T. A. (2009) Mechanisms shaping the membranes of cellular organelles. Annu. Rev. Cell Dev. Biol. 25, 329-354
34. Fukuda, M., Yamamoto, A., and Mikoshiba, K. (2001) Formation of crystalloid endoplasmic reticulum induced by expression of synaptotagmin lacking the conserved WHXL motif in the C terminus. Structural importance of the WHXL motif in the C2B domain. J. Biol. Chem. 276, 41112-41119
35. Takei, K., Mignery, G. A., Mugnaini, E., Südhof, T. C., and De Camilli, P. (1994) Inositol 1, 4, 5-trisphosphate receptor causes formation of ER cisternal stacks in transfected fibroblasts and in cerebellar Purkinje cells. Neuron 12, 327-342 (Pubitemid 24071298)
36. Yamamoto, A., Masaki, R., and Tashiro, Y. (1996) Formation of crystalloid endoplasmic reticulum in COS cells upon overexpression of microsomal aldehyde dehydrogenase by cDNA transfection. J. Cell Sci. 109, 1727-1738 (Pubitemid 26248618)
37. Lingwood, D., Schuck, S., Ferguson, C., Gerl, M. J., and Simons, K. (2009) Generation of cubic membranes by controlled homotypic interaction of membrane proteins in the endoplasmic reticulum. J. Biol. Chem. 284, 12041-12048
38. Mullins, C., and Springer Link (Online service). (2005) The Biogenesis of Cellular Organelles, in Molecular Biology Intelligence Unit, Eurekah.com and Kluwer Academic, Plenum Publishers, Boston, MA
39. Vander Heyden, A. B., Naismith, T. V., Snapp, E. L., and Hanson, P. I. (2011) Static retention of the lumenal monotopic membrane protein torsinA in the endoplasmic reticulum. EMBO J. 30, 3217-3231
40. Anderson, R. G., Orci, L., Brown, M. S., Garcia-Segura, L. M., and Goldstein, J. L. (1983) Ultrastructural analysis of crystalloid endoplasmic reticulum in UT-1 cells and its disappearance in response to cholesterol. J. Cell Sci. 63, 1-20 (Pubitemid 13020329)