Membrane docking of the C2 domain from protein kinase Cα as seen by polarized ATR-IR. the role of PIP2

Biochimica et Biophysica Acta - Biomembranes

Volumn 1808, Issue 3, 2011, Pages 684-695

  Ausili, Alessio ^a   Corbalán García, Senena ^a   Gómez Fernández, Juan C ^a   Marsh, Derek ^b  

^a UNIVERSITY OF MURCIA   (Spain)

^b MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

2 OLEOYL 1 PALMITOYLPHOSPHATIDYLCHOLINE; 2 OLEOYL 1 PALMITOYLPHOSPHATIDYLSERINE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHATIDYLSERINE; PHOSPHOLIPASE A2; PROTEIN KINASE C ALPHA; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; ATTENUATED TOTAL INTERNAL REFLECTION INFRARED SPECTROSCOPY; BETA SHEET; CRYSTAL STRUCTURE; CYTOSOL; ENZYME ACTIVATION; INFRARED SPECTROSCOPY; LIPID RAFT; MOLECULAR DOCKING; PHOSPHOLIPID MEMBRANE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE;

CELL MEMBRANE; CYTOSOL; HUMANS; MODELS, MOLECULAR; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLSERINES; PHOSPHOLIPASES A2; PROTEIN KINASE C-ALPHA; PROTEIN STRUCTURE, TERTIARY; SPECTROPHOTOMETRY, INFRARED; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

EID: 78650627501     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2010.11.035     Document Type: Article

References (68)

1. Y. Nishizuka The molecular heterogeneity of protein kinase C and its implications for cellular regulation Nature 334 1988 661 665
2. A.C. Newton Protein kinase C: structure, function, and regulation J. Biol. Chem. 270 1995 28495 28498
3. S. Corbalan-Garcia, and J.C. Gomez-Fernandez Protein kinase C regulatory domains: the art of decoding many different signals in membranes Biochim. Biophys. Acta 1761 2006 633 654 (Pubitemid 44177524)
4. H. Mellor, and P.J. Parker The extended protein kinase C superfamily Biochem. J. 332 Pt 2 1998 281 292 (Pubitemid 28271856)
5. J. Hofmann The potential for isoenzyme-selective modulation of protein kinase C FASEB J. 11 1997 649 669 (Pubitemid 27318283)
6. W. Cho, and R.V. Stahelin Membrane binding and subcellular targeting of C2 domains Biochim. Biophys. Acta 1761 2006 838 849 (Pubitemid 44332329)
7. P. Conesa-Zamora, M.J. Lopez-Andreo, J.C. Gomez-Fernandez, and S. Corbalan-Garcia Identification of the phosphatidylserine binding site in the C2 domain that is important for PKCα activation and in vivo cell localization Biochemistry 40 2001 13898 13905 (Pubitemid 33078858)
8. 2+ bridges the C2 membrane-binding domain of protein kinase Cα directly to phosphatidylserine EMBO J. 18 1999 6329 6338 (Pubitemid 29533237)
9. W.F. Ochoa, S. Corbalan-Garcia, R. Eritja, J.A. Rodriguez-Alfaro, J.C. Gomez-Fernandez, I. Fita, and N. Verdaguer Additional binding sites for anionic phospholipids and calcium ions in the crystal structures of complexes of the C2 domain of protein kinase Cα J. Mol. Biol. 320 2002 277 291 (Pubitemid 34722218)
10. 2+/phosphatidylserine binding region of the C2 domain in the translocation of protein kinase Cα to the plasma membrane J. Biol. Chem. 278 2003 10282 10290 (Pubitemid 36800289)
11. S. Corbalan-Garcia, J.A. Rodriguez-Alfaro, and J.C. Gomez-Fernandez Determination of the calcium-binding sites of the C2 domain of protein kinase Cα that are critical for its translocation to the plasma membrane Biochem. J. 337 Pt 3 1999 513 521
12. J.A. Rodriguez-Alfaro, J.C. Gomez-Fernandez, and S. Corbalan-Garcia Role of the lysine-rich cluster of the C2 domain in the phosphatidylserine-dependent activation of PKCα J. Mol. Biol. 335 2004 1117 1129 (Pubitemid 38091614)
13. W.F. Ochoa, A. Torrecillas, I. Fita, N. Verdaguer, S. Corbalan-Garcia, and J.C. Gomez-Fernandez Retinoic acid binds to the C2-domain of protein kinase Cα Biochemistry 42 2003 8774 8779 (Pubitemid 36899821)
14. S. Corbalan-Garcia, J. Garcia-Garcia, J.A. Rodriguez-Alfaro, and J.C. Gomez-Fernandez A new phosphatidylinositol 4, 5-bisphosphate-binding site located in the C2 domain of protein kinase Cα J. Biol. Chem. 278 2003 4972 4980 (Pubitemid 36801006)
15. 2+ influx and phosphatidylinositol 4, 5-bisphosphate in differentiated PC12 cells Mol. Biol. Cell 16 2005 2848 2861 (Pubitemid 40741229)
16. 2+-dependent PtdIns(4, 5)P2 sensing domain: a new insight into an old pathway J. Mol. Biol. 362 2006 901 914 (Pubitemid 44389732)
17. 2 recognition by its C2 domain Mol. Biol. Cell 17 2006 56 66 (Pubitemid 43049461)
18. M. Guerrero-Valero, C. Ferrer-Orta, J. Querol-Audi, C. Marin-Vicente, I. Fita, J.C. Gomez-Fernandez, N. Verdaguer, and S. Corbalan-Garcia Structural and mechanistic insights into the association of PKCα-C2 domain to PtdIns(4, 5)P2 Proc. Natl Acad. Sci. USA 106 2009 6603 6607
19. M. Guerrero-Valero, C. Marin-Vicente, J.C. Gomez-Fernandez, and S. Corbalan-Garcia The C2 domains of classical PKCs are specific PtdIns(4, 5)P2-sensing domains with different affinities for membrane binding J. Mol. Biol. 371 2007 608 621 (Pubitemid 47087827)
20. C. Marin-Vicente, F.E. Nicolas, J.C. Gomez-Fernandez, and S. Corbalan-Garcia The PtdIns(4, 5)P2 ligand itself influences the localization of PKCα in the plasma membrane of intact living cells J. Mol. Biol. 377 2008 1038 1052
21. P. Conesa-Zamora, J.C. Gomez-Fernandez, and S. Corbalan-Garcia The C2 domain of protein kinase Cα is directly involved in the diacylglycerol-dependent binding of the C1 domain to the membrane Biochim. Biophys. Acta 1487 2000 246 254
22. J. Garcia-Garcia, S. Corbalan-Garcia, and J.C. Gomez-Fernandez Effect of calcium and phosphatidic acid binding on the C2 domain of PKCα as studied by Fourier transform infrared spectroscopy Biochemistry 38 1999 9667 9675
23. D. Manna, N. Bhardwaj, M.S. Vora, R.V. Stahelin, H. Lu, and W. Cho Differential roles of phosphatidylserine, PtdIns(4, 5)P2, and PtdIns(3, 4, 5)P3 in plasma membrane targeting of C2 domains. Molecular dynamics simulation, membrane binding, and cell translocation studies of the PKCα C2 domain J. Biol. Chem. 283 2008 26047 26058
24. S.C. Kohout, S. Corbalan-Garcia, J.C. Gomez-Fernandez, and J.J. Falke C2 domain of protein kinase Cα: elucidation of the membrane docking surface by site-directed fluorescence and spin labeling Biochemistry 42 2003 1254 1265 (Pubitemid 36184066)
25. 2 binding on the membrane docking geometry of PKCα C2 domain: an EPR site-directed spin-labeling and relaxation study Biochemistry 47 2008 8301 8316
26. N.J. Malmberg, D.R. Van Buskirk, and J.J. Falke Membrane-docking loops of the cPLA2 C2 domain: detailed structural analysis of the protein-membrane interface via site-directed spin-labeling Biochemistry 42 2003 13227 13240 (Pubitemid 37420676)
27. C.H. Chen, S. Malkova, S.V. Pingali, F. Long, S. Garde, W. Cho, and M.L. Schlossman Configuration of PKCα-C2 domain bound to mixed SOPC/SOPS lipid monolayers Biophys. J. 97 2009 2794 2802
28. D. Marsh Spin-label electron spin resonance and Fourier transform infrared spectroscopy for structural/dynamic measurements on ion channels Methods Enzymol. 294 1999 59 92
29. A. Ausili, A. Torrecillas, M.M. Martinez-Senac, S. Corbalan-Garcia, and J.C. Gomez-Fernandez The interaction of the Bax C-terminal domain with negatively charged lipids modifies the secondary structure and changes its way of insertion into membranes J. Struct. Biol. 164 2008 146 152
30. +-ATPase in phospholipid membranes: spin-label electron paramagnetic resonance and polarized infrared spectroscopy Biochemistry 47 2008 3937 3949 (Pubitemid 351431383)
31. D. Marsh Orientation and peptide-lipid interactions of alamethicin incorporated in phospholipid membranes: polarized infrared and spin-label EPR spectroscopy Biochemistry 48 2009 729 737
32. D. Marsh, and T. Pali Infrared dichroism from the X-ray structure of bacteriorhodopsin Biophys. J. 80 2001 305 312
33. D. Marsh, M. Muller, and F.J. Schmitt Orientation of the infrared transition moments for an α-helix Biophys. J. 78 2000 2499 2510 (Pubitemid 30313809)
34. T. Pali, and D. Marsh Tilt, twist, and coiling in β-barrel membrane proteins: relation to infrared dichroism Biophys. J. 80 2001 2789 2797 (Pubitemid 32521652)
35. D. Marsh Infrared dichroism of twisted β-sheet barrels. The structure of E. coli outer membrane proteins J. Mol. Biol. 297 2000 803 808
36. D. Marsh Dichroic ratios in polarized Fourier transform infrared for nonaxial symmetry of β-sheet structures Biophys. J. 72 1997 2710 2718 (Pubitemid 27227606)
37. D. Marsh Nonaxiality in infrared dichroic ratios of polytopic transmembrane proteins Biophys. J. 75 1998 354 358 (Pubitemid 28311821)
38. D. Marsh Infrared dichroism of isotope-edited α-helices and β-sheets J. Mol. Biol. 338 2004 353 367 (Pubitemid 38447091)
39. M. Ramakrishnan, J. Qu, C.L. Pocanschi, J.H. Kleinschmidt, and D. Marsh Orientation of β-barrel proteins OmpA and FhuA in lipid membranes. Chain length dependence from infrared dichroism Biochemistry 44 2005 3515 3523 (Pubitemid 40322021)
40. J.A. Richard, I. Kelly, D. Marion, M. Pezolet, and M. Auger Interaction between β-Purothionin and dimyristoylphosphatidylglycerol: a (31)P-NMR and infrared spectroscopic study Biophys. J. 83 2002 2074 2083
41. V. Anbazhagan, J. Qu, J.H. Kleinschmidt, and D. Marsh Incorporation of outer membrane protein OmpG in lipid membranes: protein-lipid interactions and β-barrel orientation Biochemistry 47 2008 6189 6198 (Pubitemid 351812831)
42. V. Anbazhagan, N. Vijay, J.H. Kleinschmidt, and D. Marsh Protein-lipid interactions with Fusobacterium nucleatum major outer membrane protein FomA: spin-label EPR and polarized infrared spectroscopy Biochemistry 47 2008 8414 8423
43. A. Torrecillas, S. Corbalan-Garcia, and J.C. Gomez-Fernandez Structural study of the C2 domains of the classical PKC isoenzymes using infrared spectroscopy and two-dimensional infrared correlation spectroscopy Biochemistry 42 2003 11669 11681 (Pubitemid 37243627)
44. E.A. Nalefski, T. McDonagh, W. Somers, J. Seehra, J.J. Falke, and J.D. Clark Independent folding and ligand specificity of the C2 calcium-dependent lipid binding domain of cytosolic phospholipase A2 J. Biol. Chem. 273 1998 1365 1372 (Pubitemid 28133654)
45. U.P. Fringeli, and H.H. Gunthard Infrared membrane spectroscopy Mol. Biol. Biochem. Biophys. 31 1981 270 332
46. D. Marsh Quantitation of secondary structure in ATR infrared spectroscopy Biophys. J. 77 1999 2630 2637 (Pubitemid 29519507)
47. S.C. Kohout, S. Corbalan-Garcia, A. Torrecillas, J.C. Gomez-Fernandez, and J.J. Falke C2 domains of protein kinase C isoforms α, β, and γ: activation parameters and calcium stoichiometries of the membrane-bound state Biochemistry 41 2002 11411 11424
48. J.L. Arrondo, A. Muga, J. Castresana, and F.M. Goni Quantitative studies of the structure of proteins in solution by Fourier-transform infrared spectroscopy Prog. Biophys. Mol. Biol. 59 1993 23 56
49. S. Krimm, and J. Bandekar Vibrational spectroscopy and conformation of peptides, polypeptides, and proteins Adv. Protein Chem. 38 1986 181 364
50. A. Barth The infrared absorption of amino acid side chains Prog. Biophys. Mol. Biol. 74 2000 141 173 (Pubitemid 32168153)
51. W.K. Surewicz, and H.H. Mantsch New insight into protein secondary structure from resolution-enhanced infrared spectra Biochim. Biophys. Acta 952 1988 115 130 (Pubitemid 18027334)
52. G.Y. Xu, T. McDonagh, H.A. Yu, E.A. Nalefski, J.D. Clark, and D.A. Cumming Solution structure and membrane interactions of the C2 domain of cytosolic phospholipase A2 J. Mol. Biol. 280 1998 485 500 (Pubitemid 28327285)
53. E. Goormaghtigh, V. Raussens, and J.M. Ruysschaert Attenuated total reflection infrared spectroscopy of proteins and lipids in biological membranes Biochim. Biophys. Acta 1422 1999 105 185 (Pubitemid 29313327)
54. A. Torrecillas, M.M. Martinez-Senac, E. Goormaghtigh, A. de Godos, S. Corbalan-Garcia, and J.C. Gomez-Fernandez Modulation of the membrane orientation and secondary structure of the C-terminal domains of Bak and Bcl-2 by lipids Biochemistry 44 2005 10796 10809 (Pubitemid 41153640)
55. E.G. Hutchinson, and J.M. Thornton PROMOTIF - a program to identify and analyze structural motifs in proteins Protein Sci. 5 1996 212 220 (Pubitemid 26054277)
56. O. Perisic, S. Fong, D.E. Lynch, M. Bycroft, and R.L. Williams Crystal structure of a calcium-phospholipid binding domain from cytosolic phospholipase A2 J. Biol. Chem. 273 1998 1596 1604 (Pubitemid 28133685)
57. N.J. Malmberg, and J.J. Falke Use of EPR power saturation to analyze the membrane-docking geometries of peripheral proteins: applications to C2 domains Annu. Rev. Biophys. Biomol. Struct. 34 2005 71 90 (Pubitemid 40847719)
58. N.J. Malmberg Spectroscopic characterization of membrane docking C2 domains 2004 University of Colorado Boulder 167
59. B.G. Dzikovski, V.A. Livshits, and D. Marsh Oxygen permeation profile in lipid membranes: comparison with transmembrane polarity profile Biophys. J. 85 2003 1005 1012 (Pubitemid 36909664)
60. D. Marsh, B.G. Dzikovski, and V.A. Livshits Oxygen profiles in membranes Biophys. J. 90 2006 L49 L51
61. R.V. Stahelin, J.D. Rafter, S. Das, and W. Cho The molecular basis of differential subcellular localization of C2 domains of protein kinase C-α and group IVa cytosolic phospholipase A2 J. Biol. Chem. 278 2003 12452 12460 (Pubitemid 36800232)
62. 2+ affinity Biochemistry 46 2007 4322 4336 (Pubitemid 46559398)
63. J.P. Bradshaw, R.J. Bushby, C.C. Giles, and M.R. Saunders Orientation of the headgroup of phosphatidylinositol in a model biomembrane as determined by neutron diffraction Biochemistry 38 1999 8393 8401
64. A.I. Kishore, and J.H. Prestegard Molecular orientation and conformation of phosphatidylinositides in membrane mimetics using variable angle sample spinning (VASS) NMR Biophys. J. 85 2003 3848 3857 (Pubitemid 37490294)
65. 2+ Structure 6 1998 1395 1405 (Pubitemid 28541883)
66. T. Heimburg, B. Angerstein, and D. Marsh Binding of peripheral proteins to mixed lipid membranes: effect of lipid demixing upon binding Biophys. J. 76 1999 2575 2586 (Pubitemid 29264617)
67. B. Bechinger, J.M. Ruysschaert, and E. Goormaghtigh Membrane helix orientation from linear dichroism of infrared attenuated total reflection spectra Biophys. J. 76 1999 552 563 (Pubitemid 29202483)
68. 2H-NMR study and molecular dynamics simulation of the location, alignment, and mobility of pyrene in POPC bilayers Biophys. J. 88 2005 1818 1827 (Pubitemid 40976195)