Membrane docking geometry of GRP1 PH domain bound to a target lipid bilayer: An EPR site-directed spin-labeling and relaxation study

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Chen, Huai Chun ^a   Ziemba, Brian P ^a   Landgraf, Kyle E ^a   Corbin, John A ^a   Falke, Joseph J ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENERAL RECEPTOR FOR PHOSPHOINOSITIDE 1; GLUTATHIONE TRANSFERASE; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; UNCLASSIFIED DRUG;

ARTICLE; CALIBRATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELECTRON SPIN RESONANCE; ENZYME SPECIFICITY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GEOMETRY; HUMAN; LIPID BILAYER; MEMBRANE BINDING; MOLECULAR DOCKING; PHOSPHOLIPID VESICLE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN LIPID INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; RELAXATION TRAINING; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; SPIN LABELING;

CELL MEMBRANE; ELECTRON SPIN RESONANCE SPECTROSCOPY; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; KINETICS; LIPID BILAYERS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

EID: 84859137660     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0033640     Document Type: Article

References (51)

1. Lemmon MA, Ferguson KM, (2000) Signal-dependent membrane targeting by pleckstrin homology (PH) domains. Biochem J 350 Pt 1: 1-18.
2. Czech MP, (2000) PIP2 and PIP3: complex roles at the cell surface. Cell 100: 603-606.
3. Insall RH, Weiner OD, (2001) PIP3, PIP2, and cell movement-similar messages, different meanings? Dev Cell 1: 743-747.
4. Vanhaesebroeck B, Leevers SJ, Ahmadi K, Timms J, Katso R, et al. (2001) Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem 70: 535-602.
5. Wang F, Herzmark P, Weiner OD, Srinivasan S, Servant G, et al. (2002) Lipid products of PI(3)Ks maintain persistent cell polarity and directed motility in neutrophils. Nat Cell Biol 4: 513-518.
6. Czech MP, (2003) Dynamics of phosphoinositides in membrane retrieval and insertion. Annu Rev Physiol 65: 791-815.
7. DiNitto JP, Cronin TC, Lambright DG, (2003) Membrane recognition and targeting by lipid-binding domains. Sci STKE 2003: re16.
8. Corbin JA, Dirkx RA, Falke JJ, (2004) GRP1 pleckstrin homology domain: activation parameters and novel search mechanism for rare target lipid. Biochemistry 43: 16161-16173.
9. Hennessy BT, Smith DL, Ram PT, Lu Y, Mills GB, (2005) Exploiting the PI3K/AKT pathway for cancer drug discovery. Nat Rev Drug Discov 4: 988-1004.
10. Hurley JH, (2006) Membrane binding domains. Biochim Biophys Acta 1761: 805-811.
11. Hawkins PT, Anderson KE, Davidson K, Stephens LR, (2006) Signalling through Class I PI3Ks in mammalian cells. Biochem Soc Trans 34: 647-662.
12. Newton AC, (2009) Lipid activation of protein kinases. J Lipid Res 50 (Suppl): S266-271.
13. Fayard E, Xue G, Parcellier A, Bozulic L, Hemmings BA, (2010) Protein kinase B (PKB/Akt), a key mediator of the PI3K signaling pathway. Curr Top Microbiol Immunol 346: 31-56.
14. Vadas O, Burke JE, Zhang X, Berndt A, Williams RL, (2011) Structural basis for activation and inhibition of class I phosphoinositide 3-kinases. Sci Signal 4.
15. Finn RD, Mistry J, Tate J, Coggill P, Heger A, et al. (2010) The Pfam protein families database. Nucleic Acids Res 38: D211-222.
16. Calleja V, Laguerre M, Larijani B, (2009) 3-D structure and dynamics of protein kinase B-new mechanism for the allosteric regulation of an AGC kinase. J Chem Biol 2: 11-25.
17. Calleja V, Alcor D, Laguerre M, Park J, Vojnovic B, et al. (2007) Intramolecular and intermolecular interactions of protein kinase B define its activation in vivo. PLoS Biol 5: e95.
18. Okuzumi T, Fiedler D, Zhang C, Gray DC, Aizenstein B, et al. (2009) Inhibitor hijacking of Akt activation. Nat Chem Biol 5: 484-493.
19. Wu WI, Voegtli WC, Sturgis HL, Dizon FP, Vigers GP, et al. (2010) Crystal structure of human AKT1 with an allosteric inhibitor reveals a new mode of kinase inhibition. PLoS One 5: e12913.
20. Carpten JD, Faber AL, Horn C, Donoho GP, Briggs SL, et al. (2007) A transforming mutation in the pleckstrin homology domain of AKT1 in cancer. Nature 448: 439-444.
21. Lindhurst MJ, Sapp JC, Teer JK, Johnston JJ, Finn EM, et al. (2011) A mosaic activating mutation in AKT1 associated with the Proteus syndrome. N Engl J Med 365: 611-619.
22. Lietzke SE, Bose S, Cronin T, Klarlund J, Chawla A, et al. (2000) Structural basis of 3-phosphoinositide recognition by pleckstrin homology domains. Mol Cell 6: 385-394.
23. Lumb CN, He J, Xue Y, Stansfield PJ, Stahelin RV, et al. (2011) Biophysical and computational studies of membrane penetration by the GRP1 pleckstrin homology domain. Structure 19: 1338-1346.
24. Landgraf KE, Pilling C, Falke JJ, (2008) Molecular mechanism of an oncogenic mutation that alters membrane targeting: Glu17Lys modifies the PIP lipid specificity of the AKT1 PH domain. Biochemistry 47: 12260-12269.
25. Pilling C, Landgraf KE, Falke JJ, (2011) The GRP1 PH domain, like the AKT1 PH domain, possesses a sentry glutamate residue essential for specific targeting to plasma membrane PI(3,4,5)P(3). Biochemistry 50: 9845-9856.
26. Knight JD, Falke JJ, (2009) Single-molecule fluorescence studies of a PH domain: new insights into the membrane docking reaction. Biophys J 96: 566-582.
27. Knight JD, Lerner MG, Marcano-Velazquez JG, Pastor RW, Falke JJ, (2010) Single molecule diffusion of membrane-bound proteins: window into lipid contacts and bilayer dynamics. Biophys J 99: 2879-2887.
28. Jackson TR, Kearns BG, Theibert AB, (2000) Cytohesins and Centaurins: Mediators of PI 3-Kinase Regulated Arf Signaling. Trends in Biochemical Science 25: 489-495.
29. Cohen LA, Honda A, Varnai P, Brown FD, Balla T, et al. (2007) Active Arf6 Recruits ARNO/Cytohesin GEFs to the PM by Binding Their PH Domains. Molecular Biology of the Cell 18: 2244-2253.
30. Park WS, Heo WD, Whalen JH, O'Rourke NA, Bryan HM, et al. (2008) Comprehensive identification of PIP3-regulated PH domains from C. elegans to H. sapiens by model prediction and live imaging. Mol Cell 30: 381-392.
31. Altenbach C, Greenhalgh DA, Khorana HG, Hubbell WL, (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 U S A 91: 1667-1671.
32. Yu YG, Thorgeirsson TE, Shin YK, (1994) Topology of an amphiphilic mitochondrial signal sequence in the membrane-inserted state: a spin labeling study. Biochemistry 33: 14221-14226.
33. Ball A, Nielsen R, Gelb MH, Robinson BH, (1999) Interfacial membrane docking of cytosolic phospholipase A2 C2 domain using electrostatic potential-modulated spin relaxation magnetic resonance. Proc Natl Acad Sci U S A 96: 6637-6642.
34. Frazier AA, Wisner MA, Malmberg NJ, Victor KG, Fanucci GE, et al. (2002) Membrane orientation and position of the C2 domain from cPLA2 by site-directed spin labeling. Biochemistry 41: 6282-6292.
35. Frazier AA, Roller CR, Havelka JJ, Hinderliter A, Cafiso DS, (2003) Membrane-bound orientation and position of the synaptotagmin I C2A domain by site-directed spin labeling. Biochemistry 42: 96-105.
36. Malmberg NJ, Van Buskirk DR, Falke JJ, (2003) Membrane-docking loops of the cPLA2 C2 domain: detailed structural analysis of the protein-membrane interface via site-directed spin-labeling. Biochemistry 42: 13227-13240.
37. Malmberg NJ, Falke JJ, (2005) Use of EPR power saturation to analyze the membrane-docking geometries of peripheral proteins: applications to C2 domains. Annu Rev Biophys Biomol Struct 34: 71-90.
38. Rufener E, Frazier AA, Wieser CM, Hinderliter A, Cafiso DS, (2005) Membrane-bound orientation and position of the synaptotagmin C2B domain determined by site-directed spin labeling. Biochemistry 44: 18-28.
39. Herrick DZ, Sterbling S, Rasch KA, Hinderliter A, Cafiso DS, (2006) Position of synaptotagmin I at the membrane interface: cooperative interactions of tandem C2 domains. Biochemistry 45: 9668-9674.
40. Landgraf KE, Malmberg NJ, Falke JJ, (2008) Effect of PIP2 binding on the membrane docking geometry of PKC alpha C2 domain: an EPR site-directed spin-labeling and relaxation study. Biochemistry 47: 8301-8316.
41. Kuo W, Herrick DZ, Ellena JF, Cafiso DS, (2009) The calcium-dependent and calcium-independent membrane binding of synaptotagmin 1: two modes of C2B binding. J Mol Biol 387: 284-294.
42. Kuo W, Herrick DZ, Cafiso DS, (2011) Phosphatidylinositol 4,5-bisphosphate alters synaptotagmin 1 membrane docking and drives opposing bilayers closer together. Biochemistry 50: 2633-2641.
43. Jaud S, Tobias DJ, Falke JJ, White SH, (2007) Self-induced docking site of a deeply embedded peripheral membrane protein. Biophys J 92: 517-524.
44. Li Z, Venable RM, Rogers LA, Murray D, Pastor RW, (2009) Molecular dynamics simulations of PIP2 and PIP3 in lipid bilayers: determination of ring orientation, and the effects of surface roughness on a Poisson-Boltzmann description. Biophys J 97: 155-163.
45. Frazier AA, Wisner MA, Malmberg NJ, Victor KG, Fanucci GE, et al. (2002) Membrane orientation and position of the C2 domain from cPLA2 by site-directed spin labeling. Biochemistry 41: 6282-92 Erratum in: Biochemistry 41:7528.
46. Lai CL, Landgraf KE, Voth GA, Falke JJ, (2010) Membrane docking geometry and target lipid stoichiometry of PKCalpha C2 domain: A combined molecular dynamics and experimental study. J Mol Biol 402: 301-310.
47. Langen R, Oh KJ, Cascio D, Hubbell WL, (2000) Crystal structures of spin labeled T4 lysozyme mutants: implications for the interpretation of EPR spectra in terms of structure. Biochemistry 39: 8396-8405.
48. Wiener MC, White SH, (1992) Structure of a fluid dioleoylphosphatidylcholine bilayer determined by joint refinement of x-ray and neutron diffraction data. III. Complete structure. Biophys J 61: 434-447.
49. Yau WM, Wimley WC, Gawrisch K, White SH, (1998) The preference of tryptophan for membrane interfaces. Biochemistry 37: 14713-14718.
50. Hoff B, Strandberg E, Ulrich AS, Tieleman DP, Posten C, (2005) 2H-NMR study and molecular dynamics simulation of the location, alignment, and mobility of pyrene in POPC bilayers. Biophys J 88: 1818-1827.
51. Ziemba BP, Knight JD, Falke JJ, (2012) Assembly of membrane-bound protein complexes: Detection and analysis by single molecule diffusion. Biochemistry in press.