Assessment of GABARAP self-association by its diffusion properties

Journal of Biomolecular NMR

Volumn 48, Issue 1, 2010, Pages 49-58

  Pacheco, Victor ^a   Ma, Peixiang ^a   Thielmann, Yvonne ^a,c   Hartmann, Rudolf ^a   Weiergräber, Oliver H ^a   Mohrlüder, Jeannine ^a   Willbold, Dieter ^a,b  

^a FORSCHUNGSZENTRUM JÜLICH   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

Author keywords

Diffusion ordered spectroscopy; GABARAP; NMR spectroscopy; Protein oligomerization

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; DIMER; GAMMA AMINOBUTYRIC ACID A RECEPTOR ASSOCIATED PROTEIN; MONOMER; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHAGY; DIFFUSION; HETERONUCLEAR SINGLE QUANTUM COHERENCE; HUMAN; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN CONFORMATION; TEMPERATURE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; DIFFUSION; HUMANS; MICROTUBULE-ASSOCIATED PROTEINS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN MULTIMERIZATION; TEMPERATURE;

EID: 77956479326     PISSN: 09252738     EISSN: 15735001     Source Type: Journal    
DOI: 10.1007/s10858-010-9437-5     Document Type: Article

References (52)

1. AS Altieri DP Hinton RA Byrd 1995 Association of biomolecular systems via pulsed field gradient NMR self diffusion measurements J Am Chem Soc 117:7566-7567 10.1021/ja00133a039
2. B Antalek 2002 Using pulsed gradient spin echo NMR for chemical mixtures analysis: How to obtain optimal results Concepts Magn Reson 14:225-258 10.1002/cmr.10026
3. A-receptor-associated protein, GABARAP EMBO Rep 3:183-189 10.1093/embo-reports/kvf026 (Pubitemid 34213498)
4. Berne BJ, Pecora R (2000) Dynamic light scattering with applications to chemistry, biology and physics. Dover Publications, New York
5. T Brand EJ Cabrita GA Morris R Günther HJ Hofmann S Berger 2007 Residue-specific NH exchange rates studied by NMR diffusion experiments J Magn Reson 187:97-104 10.1016/j.jmr.2007.03.021 2007JMagR.187..97B (Pubitemid 46908780)
6. A receptor localization and tubulin binding Neuron 33:63-74 10.1016/S0896-6273(01)00558-X (Pubitemid 34088179)
7. Deslauriers R, Smith CP (1981) The multinuclear NMR approach to peptides: structures, conformations, and dynamics. In: Berliner JL, Reuben J (eds) Biological magnetic resonance. Plenum Press, New York, pp 243-344
8. AJ Dingley JP Mackay BE Chapman MB Morris PW Kuchel BD Hambly GF King 1995 Measuring protein self-association using pulsed-field-gradient NMR spectroscopy: application to myosin light chain 2 J Biomol NMR 6:321-328 10.1007/BF00197813
9. Enna SJ, Möhler H (2007) The GABA receptors, 3rd edn. Humana Press, Totowa
10. Glatter O, Kratky O (1982) Small angle X-ray scattering. Academic Press, London
11. 1H and less-common nuclei J Magn Reson 92 115 125
12. CS Johnson Jr 1999 Diffusion ordered nuclear magnetic resonance spectroscopy: principles and applications Prog Nucl Magn Reson Spectrosc 34:203-256 10.1016/S0079-6565(99)00003-5 1999sbmg.book...J
13. JA Jones DK Wilkins LJ Smith CM Dobson 1997 Characterisation of protein unfolding by NMR diffusion measurements J Biomol NMR 10:199-203 10.1023/A:1018304117895
14. Y Kabeya N Mizushima A Yamamoto S Oshitani-Okamoto Y Ohsumi T Yoshimori 2004 LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation J Cell Sci 117:2805-2812 10.1242/jcs.01131 (Pubitemid 38997262)
15. M Kataoka Y Goto 1996 X-ray solution scattering studies of protein folding Fold Des 1 R107 R114 10.1016/S1359-0278(96)00047-8
16. A receptors at synaptic sites Brain Res Rev 39:74-83 10.1016/S0165-0173(02)00159-5 (Pubitemid 34666987)
17. D Knight R Harris MS McAlister JP Phelan S Geddes SJ Moss PC Driscoll NH Keep 2002 The X-ray crystal structure and putative ligand-derived peptide binding properties of gamma-aminobutyric acid receptor type A receptor-associated protein J Biol Chem 277:5556-5561 10.1074/jbc.M109753200 (Pubitemid 34968607)
18. R Koradi M Billeter K Wüthrich 1996 MOLMOL: a program for display and analysis of macromolecular structures J Mol Graph 14:51-55 10.1016/0263-7855(96)00009-4 (Pubitemid 26152976)
19. A receptor associated protein J Biomol NMR 22:97-98 10.1023/A:1013884402033 (Pubitemid 34157076)
20. EE Lattman 1994 Small angle scattering studies of protein folding Curr Opin Struct Biol 4:87-92 10.1016/S0959-440X(94)90064-7
21. J Mohrlüder T Stangler Y Hoffmann K Wiesehan A Mataruga D Willbold 2007 Identification of calreticulin as a ligand of GABARAP by phage display screening of a peptide library FEBS J 274:5543-5555 10.1111/j.1742-4658.2007. 06073.x (Pubitemid 47622066)
22. J Mohrlüder Y Hoffmann T Stangler K Hänel D Willbold 2007 Identification of clathrin heavy chain as a direct interaction partner for the γ-aminobutyric acid type A receptor associated protein Biochemistry 46:14537-14543 10.1021/bi7018145 (Pubitemid 350276359)
23. J Mohrlüder M Schwarten D Willbold 2009 Structure and possible function of gamma-aminobutyrate type A receptor-associated protein FEBS J 276:4989-5005 10.1111/j.1742-4658.2009.07207.x
24. SJ Moss TG Smart 2001 Constructing inhibitory synapses Nat Rev Neurosci 2:240-250 10.1038/35067500 (Pubitemid 33673065)
25. H Nakatogawa Y Ichimura Y Ohsumi 2007 Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion Cell 130:165-178 10.1016/j.cell.2007.05.021 (Pubitemid 47031316)
26. NN Noda H Kumeta H Nakatogawa K Satoo W Adachi J Ishii Y Fujioka Y Ohsumi F Inagaki 2008 Structural basis of target recognition by Atg8/LC3 during selective autophagy Genes Cells 13:1211-1218 10.1111/j.1365-2443.2008.01238.x
27. A receptor-associated protein (GABARAP) mediating dimer formation Neuropharmacology 43:476-481 10.1016/S0028-3908(02) 00165-X (Pubitemid 35279559)
28. A receptors J Neurochem 80:815-823 10.1046/j.0022-3042.2002.00762.x (Pubitemid 34809234)
29. H Pan G Barany C Woodward 1997 Reduced BPTI is collapsed. A pulsed field gradient NMR study of unfolded and partially folded bovine pancreatic trypsin inhibitor Protein Sci 6:1985-1992 10.1002/pro.5560060919
30. Y Paz Z Elazar D Fass 2000 Structure of GATE-16, membrane transport modulator and mammalian ortholog of autophagocytosis factor Aut7p J Biol Chem 275:25445-25450 10.1074/jbc.C000307200
31. WS Price 1997 Pulsed-field gradient nuclear magnetic resonance as a tool for studying translational diffusion: Part I. Basic Theory Concepts Magn Reson 9:299-336 10.1002/(SICI)1099-0534(1997)9:5<299::AID-CMR2>3.0.CO;2-U (Pubitemid 127116750)
32. WS Price 1998 Pulsed-field gradient nuclear magnetic resonance as a tool for studying translational diffusion: Part II. Experimental aspects Concepts Magn Reson 10:197-237 10.1002/(SICI)1099-0534(1998)10:4<197::AID-CMR1>3.0. CO;2-S (Pubitemid 128089836)
33. WS Price F Tsuchiya Y Arata 1999 Lysozyme aggregation and solution properties studied using PGSE NMR diffusion measurements J Am Chem Soc 121:11503-11512 10.1021/ja992265n (Pubitemid 30010481)
34. FM Richards 1974 The interpretation of protein structures: total volume, group volume distributions and packing density J Mol Biol 82:1-14 10.1016/0022-2836(74)90570-1
35. K Satoo NN Noda H Kumeta Y Fujioka Y Ohsumi F Inagaki 2009 The structure of Atg4B-LC3 complex reveals the mechanism of LC3 processing and delipidation during autophagy EMBO J 28:1341-1350 10.1038/emboj.2009.80
36. M Schwarten J Mohrlüder P Ma M Stoldt Y Thielmann T Stangler N Hersch B Hoffmann R Merkel D Willbold 2009 Nix directly binds to GABARAP: a possible crosstalk between apoptosis and autophagy Autophagy 5:690-698 10.4161/auto.5.5.8494
37. YS Sou I Tanida M Komatsu T Ueno E Kominami 2006 Phosphatidylserine in addition to phosphatidylethanolamine is an in vitro target of the mammalian Atg8 modifiers, LC3, GABARAP, and GATE-16 J Biol Chem 281:3017-3024 10.1074/jbc.M505888200 (Pubitemid 43845910)
38. 15N resonance assignments of human GABA receptor associated protein J Biomol NMR 21:183-184 10.1023/A:1012416810974 (Pubitemid 33040169)
39. A receptor-associated protein GABARAP: implications for biological function and its regulation J Biol Chem 277:13363-13366 10.1074/jbc.C200050200 (Pubitemid 34967926)
40. K Sugawara NN Suzuki Y Fujioka N Mizushima Y Ohsumi F Inagaki 2004 The crystal structure of microtubule-associated protein light chain 3, a mammalian homologue of Saccharomyces cerevisiae Atg8 Genes Cells 9:611-618 10.1111/j.1356-9597.2004.00750.x (Pubitemid 39117535)
41. I Tanida M Komatsu T Ueno E Kominami 2003 GATE-16 and GABARAP are authentic modifiers mediated by Apg7 and Apg3 Biochem Biophys Res Commun 300:637-644 10.1016/S0006-291X(02)02907-8 (Pubitemid 36268883)
42. A receptor-associated protein-phospholipid conjugates J Biol Chem 279:36268-36276 10.1074/jbc.M401461200 (Pubitemid 39128963)
43. Y Thielmann J Mohrlüder BW Koenig T Stangler R Hartmann K Becker H-D Höltje D Willbold 2008 An indole-binding site is a major determinant of the ligand specificity of the GABA type A receptor-associated protein GABARAP ChemBioChem 11:1767-1775 10.1002/cbic.200800117
44. Y Thielmann OH Weiergräber J Mohrlüder D Willbold 2009 Structural framework of the GABARAP-calreticulin interface-implications for substrate binding to endoplasmic reticulum chaperones FEBS J 276:1140-1152 10.1111/j.1742-4658.2008.06857.x
45. Y Thielmann OH Weiergräber P Ma M Schwarten J Mohrlüder D Willbold 2009 Comparative modeling of human NSF reveals a possible binding site for GABARAP and GATE-16 Proteins 77:637-646 10.1002/prot.22477
46. Y Thielmann OH Weiergräber J Mohrlüder D Willbold 2009 Structural characterization of GABARAP-ligand interactions Mol Biosyst 5:575-579 10.1039/b900425d
47. A receptors and the cytoskeleton Nature 397:69-72 10.1038/16264 1999Natur.397..69W (Pubitemid 29038250)
48. H Weidberg E Shvets T Shpilka F Shimron V Shinder Z Elazar 1999 LC3 and GATE-16/GABARAP subfamilies are both essential yet act differently in autophagosome biogenesis EMBO J 29:1792-1802 10.1038/emboj.2010.74
49. A receptor-associated protein J Mol Biol 381:1320-1331 10.1016/j.jmb.2008.06.086
50. H Weingärtner M Holz 2002 NMR studies of self-diffusion in liquids Annu Rep Prog Chem Sect C 98 121 155
51. PR Wills Y Georgialis 1981 Concentration dependence of the diffusion coefficient of a dimerizing protein: bovine pancreatic trypsin inhibitor J Phys Chem 85:3978-3984 10.1021/j150626a006
52. D Wu A Chen CS Johnson Jr 1995 An improved diffusion-ordered spectroscopy experiment incorporating bipolar-gradient pulses J Magn Reson A115 260 264