Interactions of the GM2 activator protein with phosphatidylcholine bilayers: A site-directed spin-labeling power saturation study

Biophysical Journal

Volumn 97, Issue 5, 2009, Pages 1436-1444

  Mathias, Jordan D ^a   Ran, Yong ^a   Carter, Jeffery D ^a   Fanucci, Gail E ^a  

^a University of Florida   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GANGLIOSIDE GM2 ACTIVATOR PROTEIN; LIPID; PHOSPHATIDYLCHOLINE;

ARTICLE; CELL SURFACE; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; LIPID BILAYER; PROTEIN BINDING; PROTEIN INTERACTION; SPIN LABELING;

CHELATING AGENTS; ELECTRON SPIN RESONANCE SPECTROSCOPY; G(M2) ACTIVATOR PROTEIN; LIPID BILAYERS; MODELS, CHEMICAL; MODELS, MOLECULAR; MUTATION; NICKEL; PHOSPHATIDYLCHOLINES; RECOMBINANT PROTEINS; SPIN LABELS; WATER;

EID: 70349605641     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.05.058     Document Type: Article

References (35)

1. Gravel, R., J. Clarke, M. Kaback, D. Mahuran, K. Sandhoff, et al. 1995. The GM2 Gangliosidoses C. R. Scriver, A. L. Beaudet, W. S. Sly, and D. Valle, editors. McGraw-Hill, New York.
2. Sandhoff, K., and T. Kolter. 1996. Topology of glycosphingolipid degradation. Trends Cell Biol. 6:98-103.
3. Kolter, T., and K. Sandhoff. 2005. Principles of lysosomal membrane digestion: stimulation of sphingolipid degradation by sphingolipid activator proteins and anionic lysosomal lipids. Annu. Rev. Cell Dev. Biol. 21:81-103.
4. Fürst, W., and K. Sandhoff. 1992. Activator proteins and topology of lysosomal sphingolipid catabolism. Biochim. Biophys. Acta. 1126:1-16.
5. Wright, C. S., S. C. Li, and F. Rastinejad. 2000. Crystal structure of human GM2-activator protein with a novel β-cup topology. J. Mol. Biol. 304:411-422.
6. Wright, C. S., L. Z. Mi, and F. Rastinejad. 2004. Evidence for lipid packaging in the crystal structure of the GM2-activator complex with platelet activating factor. J. Mol. Biol. 342:585-592.
7. Wright, C. S., L. Z. Mi, S. Lee, and F. Rastinejad. 2005. Crystal structure analysis of phosphatidylcholine-GM2-activator product complexes: evidence for hydrolase activity. Biochemistry. 44:13510-13521.
8. Conzelmann, E., J. Burg, G. Stephan, and K. Sandhoff. 1982. Complexing of glycolipids and their transfer between membranes by the activator protein for degradation of lysosomal ganglioside GM2. Eur. J. Biochem. 123:455-464.
9. Mahuran, D. J. 1998. The GM2 activator protein, its roles as a co-factor in GM2 hydrolysis and as a general glycolipid transport protein. Biochim. Biophys. Acta. 1393:1-18.
10. Rigat, B., W. Wang, A. Leung, and D. J. Mahuran. 1997. Two mechanisms for the recapture of extracellular GM2 activator protein: evidence for a major secretory form of the protein. Biochemistry. 36:8325-8331. (Pubitemid 27297543)
11. Ran, Y., and G. E. Fanucci. 2008. A dansyl fluorescence-based assay for monitoring kinetics of lipid extraction and transfer. Anal. Biochem. 382:132-134.
12. Giehl, A., T. Lemm, O. Bartelsen, K. Sandhoff, and A. Blume. 1999. Interaction of the GM2-activator protein with phospholipid-ganglioside bilayer membranes and with monolayers at the air-water interface. Eur. J. Biochem. 261:650-658.
13. Altenbach, C., D. A. Greenhalgh, H. G. Khorana, and W. L. Hubbell. 1994. A collision gradient method to determine the immersion depth of nitroxides in lipid bilayers: application to spin-labeled mutants of bacteriorhodopsin. Proc. Natl. Acad. Sci. USA. 91:1667-1671.
14. Frazier, A. A., C. R. Roller, J. J. Havelka, A. Hinderliter, and D. S. Cafiso. 2003. Membrane-bound orientation and position of the Synaptotagmin I C2A domain by site-directed spin labeling. Biochemistry. 42:96-105.
15. Frazier, A. A., M. A. Wisner, N. J. Malmberg, K. G. Victor, G. E. Fanucci, et al. 2002. Membrane orientation and position of the C2 domain from cPLA2 by site-directed spin labeling. Biochemistry. 41:6282-6292. (Pubitemid 34525992)
16. Gross, A., and W. L. Hubbell. 2002. Identification of protein side chains near the membrane-aqueous interface: a site-directed spin labeling study of KcsA. Biochemistry. 41:1123-1128. (Pubitemid 34083764)
17. Herrick, D. Z., S. Sterbling, K. A. Rasch, A. Hinderliter, and D. S. Cafiso. 2006. Position of Synaptotagmin I at the membrane interface: cooperative interactions of tandem C2 domains. Biochemistry. 45:9668-9674.
18. Koteiche, H. A., M. D. Reeves, and H. S. McHaourab. 2003. Structure of the substrate binding pocket of the multidrug transporter EmrE: sitedirected spin labeling of transmembrane segment 1. Biochemistry. 42:6099-6105.
19. Perozo, E., D. M. Cortes, P. Sompornpisut, A. Kloda, and B. Martinac. 2002. Open channel structure of MscL and the gating mechanism of mechanosensitive channels. Nature. 418:942-948. (Pubitemid 34976024)
20. Fanucci, G. E., and D. S. Cafiso. 2006. Recent advances and applications of site-directed spin labeling. Curr. Opin. Struct. Biol. 16:644-653.
21. Fanucci, G. E., N. Cadieux, C. A. Piedmont, R. J. Kadner, and D. S. Cafiso. 2002. Structure and dynamics of the β-barrel of the membrane transporter BtuB by site-directed spin labeling. Biochemistry. 41:11543-11551.
22. Kirby, T. L., C. B. Karim, and D. D. Thomas. 2004. Electron paramagnetic resonance reveals a large-scale conformational change in the cytoplasmic domain of phospholamban upon binding to the sarcoplasmic reticulum Ca-ATPase. Biochemistry. 43:5842-5852.
23. Dong, J., G. Yang, and H. S. McHaourab. 2005. Structural basis of energy transduction in the transport cycle of MsbA. Science. 308:1023-1028. (Pubitemid 40664413)
24. Perozo, E., D. M. Cortes, and L. G. Cuello. 1998. Three-dimensional architecture and gating mechanism of a K+ channel studied by EPR spectroscopy. Nat. Struct. Biol. 5:459-469.
25. 2 to anionic interfaces as studied by continuous wave and time domain electron paramagnetic resonance spectroscopy. J. Biol. Chem. 277:30984-30990.
26. Macosko, J. C., C. H. Kim, and Y. K. Shin. 1997. The membrane topology of the fusion peptide region of influenza hemagglutinin determined by spin-labeling EPR. J. Mol. Biol. 267:1139-1148.
27. Ran, Y., and G.E. Fanucci. Ligand extraction properties of the GM2 activator protein and its interactions with lipid vesicles. Biophys. J. 97:257-266.
28. Smirnova, T. I., T. G. Chadwick, R. MacArthur, O. Poluektov, L. Song, et al. 2006. The chemistry of phospholipid binding by the Saccharomyces cerevisiae phosphatidylinositol transfer protein Sec14p as determined by EPR spectroscopy. J. Biol. Chem. 281:34897-34908.
29. Smirnova, T. I., T. G. Chadwick, M. A. Voinov, O. Poluektov, J. van Tol, et al. 2007. Local polarity and hydrogen bonding inside the Sec14p phospholipid-binding cavity: high-field multi-frequency electron paramagnetic resonance studies. Biophys. J. 92:3686-3695.
30. McHaourab, H. S., M. A. Lietzow, K. Hideg, and W. L. Hubbell. 1996. Motion of spin-labeled side chains in T4 lysozyme. Correlation with protein structure and dynamics. Biochemistry. 35:7692-7704.
31. Hubbell, W. L., and C. Altenbach. 1994. Investigation of structure and dynamics in membrane proteins using site directed spin labeling. Curr. Opin. Struct. Biol. 4:566-573.
32. Wendeler, M., J. Hoernschemeyer, D. Hoffmann, T. Kolter, G. Schwarzmann, et al. 2004. Photoaffinity labeling of the human GM2- activator protein. Mechanistic insight into ganglioside GM2 degradation. Eur. J. Biochem. 271:614-627.
33. Wright, C. S., Q. Zhao, and F. Rastinejad. 2003. Structural analysis of lipid complexes of GM2-activator protein. J. Mol. Biol. 331:951-964.
34. Kuwana, T., B. M. Mullock, and J. P. Luzio. 1995. Identification of a lysosomal protein causing lipid transfer, using a fluorescence assay designed to monitor membrane fusion between rat liver endosomes and lysosomes. Biochem. J. 308:937-946.
35. Zhou, D., C. Cantu, 3rd, Y. Sagiv, N. Schrantz, A. B. Kulkarni, et al. 2004. Editing of CD1d-bound lipid antigens by endosomal lipid transfer proteins. Science. 303:523-527.