Regulation of Torsin ATPases by LAP1 and LULL1

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 17, 2013, Pages

  Zhao, Chenguang ^a   Brown, Rebecca S H ^a   Chase, Anna R ^a   Eisele, Markus R ^a   Schlieker, Christian ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

DYT1 dystonia; LINC complex; Nuclear egress

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; MEMBRANE PROTEIN; MUTANT PROTEIN; PROTEIN LAP1; PROTEIN LULL1; PROTEOLIPOSOME; TORSIN A; UNCLASSIFIED DRUG;

ARTICLE; CELL NUCLEUS MEMBRANE; CONTROLLED STUDY; DYSTONIA; ENDOPLASMIC RETICULUM; LOSS OF FUNCTION MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN HYDROLYSIS; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM;

ADENOSINE TRIPHOSPHATASES; CARRIER PROTEINS; CHROMATOGRAPHY, GEL; CLONING, MOLECULAR; DYSTONIA MUSCULORUM DEFORMANS; ENDOPLASMIC RETICULUM; HEK293 CELLS; HELA CELLS; HSC70 HEAT-SHOCK PROTEINS; HUMANS; HYDROLYSIS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MEMBRANE PROTEINS; MOLECULAR CHAPERONES;

NIA;

EID: 84876880737     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1300676110     Document Type: Article

References (40)

1. Ozelius LJ, et al. (1997) The early-onset torsion dystonia gene (DYT1) encodes an ATP-binding protein. Nat Genet 17(1):40-48.
2. 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(1):27-43.
3. Hanson PI, Whiteheart SW (2005) AAA+ proteins: Have engine, will work. Nat Rev Mol Cell Biol 6(7):519-529.
4. Atai NA, Ryan SD, Kothary R, Breakefield XO, Nery FC (2012) Untethering the nuclear envelope and cytoskeleton: biologically distinct dystonias arising from a common cellular dysfunction. Int J Cell Biol 2012:634214.
5. Kim CE, Perez A, Perkins G, Ellisman MH, Dauer WT (2010) A molecular mechanism underlying the neural-specific defect in torsinA mutant mice. Proc Natl Acad Sci USA 107(21):9861-9866.
6. Goodchild RE, Kim CE, Dauer WT (2005) Loss of the dystonia-associated protein torsinA selectively disrupts the neuronal nuclear envelope. Neuron 48(6):923-932.
7. Hewett J, et al. (2000) Mutant torsinA, responsible for early-onset torsion dystonia, forms membrane inclusions in cultured neural cells. Hum Mol Genet 9(9):1403-1413.
8. Callan AC, Bunning S, Jones OT, High S, Swanton E (2007) Biosynthesis of the dystonia-associated AAA+ ATPase torsinA at the endoplasmic reticulum. Biochem J 401(2): 607-612.
9. 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. Mol Biol Cell 20(11):2661-2672.
10. Liu Z, Zolkiewska A, Zolkiewski M (2003) Characterization of human torsinA and its dystonia-associated mutant form. Biochem J 374(Pt 1):117-122.
11. 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(16):3217-3231.
12. Gonzalez-Alegre P, Paulson HL (2004) Aberrant cellular behavior of mutant torsinA implicates nuclear envelope dysfunction in DYT1 dystonia. J Neurosci 24(11):2593-2601.
13. Goodchild RE, Dauer WT (2004) Mislocalization to the nuclear envelope: An effect of the dystonia-causing torsinA mutation. Proc Natl Acad Sci USA 101(3):847-852.
14. Naismith TV, Heuser JE, Breakefield XO, Hanson PI (2004) TorsinA in the nuclear envelope. Proc Natl Acad Sci USA 101(20):7612-7617.
15. 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(7):1267-1279.
16. 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(6):855-862.
17. Schirmer EC, Florens L, Guan T, Yates JR, 3rd, Gerace L (2003) Nuclear membrane proteins with potential disease links found by subtractive proteomics. Science 301(5638): 1380-1382.
18. Hetzer MW, Wente SR (2009) Border control at the nucleus: Biogenesis and organization of the nuclear membrane and pore complexes. Dev Cell 17(5):606-616.
19. Zhang X, et al. (2000) Structure of the AAA ATPase p97. Mol Cell 6(6):1473-1484.
20. 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(41): 27866-27874.
21. Cantor, CR, Schimmel PR (1980) Biophysical Chemistry: Part III (W. H. Freeman, San Francisco), pp 1135-1139.
22. van Meer G, Voelker DR, Feigenson GW (2008) Membrane lipids: Where they are and how they behave. Nat Rev Mol Cell Biol 9(2):112-124.
23. Davison SC, Wills ED (1974) Studies on the lipid composition of the rat liver endoplasmic reticulum after induction with phenobarbitone and 20-methylcholanthrene. Biochem J 140(3):461-468.
24. Weissman JS, Kashi Y, Fenton WA, Horwich AL (1994) GroEL-mediated protein folding proceeds by multiple rounds of binding and release of nonnative forms. Cell 78(4): 693-702.
25. Weber-Ban EU, Reid BG, Miranker AD, Horwich AL (1999) Global unfolding of a substrate protein by the Hsp100 chaperone ClpA. Nature 401(6748):90-93.
26. Schlieker C, Tews I, Bukau B, Mogk A (2004) Solubilization of aggregated proteins by ClpB/DnaK relies on the continuous extraction of unfolded polypeptides. FEBS Lett 578(3):351-356.
27. Nagy M, Wu HC, Liu Z, Kedzierska-Mieszkowska S, Zolkiewski M (2009) Walker-A threonine couples nucleotide occupancy with the chaperone activity of the AAA+ ATPase ClpB. Protein Sci 18(2):287-293.
28. Roudiak SG, Shrader TE (1998) Functional role of the N-terminal region of the Lon protease from Mycobacterium smegmatis. Biochemistry 37(32):11255-11263.
29. Asahara Y, et al. (2000) FtsH recognizes proteins with unfolded structure and hydrolyzes the carboxyl side of hydrophobic residues. J Biochem 127(5):931-937.
30. Speese SD, et al. (2012) Nuclear envelope budding enables large ribonucleoprotein particle export during synaptic Wnt signaling. Cell 149(4):832-846.
31. Rose A, Schlieker C (2012) Alternative nuclear transport for cellular protein quality control. Trends Cell Biol 22(10):509-514.
32. Johnson DC, Baines JD (2011) Herpesviruses remodel host membranes for virus egress. Nat Rev Microbiol 9(5):382-394.
33. Malhas A, Goulbourne C, Vaux DJ (2011) The nucleoplasmic reticulum: Form and function. Trends Cell Biol 21(6):362-373.
34. Hurley JH, Hanson PI (2010) Membrane budding and scission by the ESCRT machinery: It's all in the neck. Nat Rev Mol Cell Biol 11(8):556-566.
35. Henne WM, Buchkovich NJ, Emr SD (2011) The ESCRT pathway. Dev Cell 21(1):77-91.
36. Burns LT, Wente SR (2012) Trafficking to uncharted territory of the nuclear envelope. Curr Opin Cell Biol 24(3):341-349.
37. Nery FC, et al. (2008) TorsinA binds the KASH domain of nesprins and participates in linkage between nuclear envelope and cytoskeleton. J Cell Sci 121(Pt 20):3476-3486.
38. Baykov AA, Evtushenko OA, Avaeva SM (1988) A malachite green procedure for orthophosphate determination and its use in alkaline phosphatase-based enzyme immunoassay. Anal Biochem 171(2):266-270.
39. Zhao C, Haase W, Tampé R, Abele R (2008) Peptide specificity and lipid activation of the lysosomal transport complex ABCB9 (TAPL). J Biol Chem 283(25):17083-17091.
40. Quaite-Randall E, Joachimiak A (2000) Purification of GroEL from an overproducing E. coli strain. Methods Mol Biol 140:29-39.