Cooperative binding of annexin A2 to cholesterol- and phosphatidylinositol-4,5-bisphosphate-containing bilayers

Biophysical Journal

Volumn 107, Issue 9, 2014, Pages 2070-2081

  Drücker, Patrick ^a   Pejic, Milena ^a   Grill, David ^a   Galla, Hans Joachim ^a   Gerke, Volker ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANXA2 PROTEIN, HUMAN; CALCIUM; CHOLESTEROL; LIPID BILAYER; LIPOCORTIN 2; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLSERINE; PROTEIN S 100; S100 CALCIUM BINDING PROTEIN A10;

ADSORPTION; ESCHERICHIA COLI; GENETICS; HUMAN; LIPID BILAYER; METABOLISM;

ADSORPTION; ANNEXIN A2; CALCIUM; CHOLESTEROL; ESCHERICHIA COLI; HUMANS; LIPID BILAYERS; PHOSPHATIDYLINOSITOLS; PHOSPHATIDYLSERINES; S100 PROTEINS;

EID: 84908577754     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2014.08.027     Document Type: Article

References (78)

1. D. Lingwood, and K. Simons Lipid rafts as a membrane-organizing principle Science 327 2010 46 50
2. V. Gerke, and S.E. Moss Annexins: from structure to function Physiol. Rev. 82 2002 331 371
3. 2+ signalling to membrane dynamics Nat. Rev. Mol. Cell Biol. 6 2005 449 461
4. P. Raynal, and H.B. Pollard Annexins: the problem of assessing the biological role for a gene family of multifunctional calcium- and phospholipid-binding proteins Biochim. Biophys. Acta 1197 1994 63 93
5. E. Morel, and J. Gruenberg The p11/S100A10 light chain of annexin A2 is dispensable for annexin A2 association to endosomes and functions in endosomal transport PLoS ONE 2 2007 e1118
6. C. Thiel, M. Osborn, and V. Gerke The tight association of the tyrosine kinase substrate annexin II with the submembranous cytoskeleton depends on intact p11- and Ca(2+)-binding sites J. Cell Sci. 103 1992 733 742
7. N. Johnsson, G. Marriott, and K. Weber p36, the major cytoplasmic substrate of src tyrosine protein kinase, binds to its p11 regulatory subunit via a short amino-terminal amphiphatic helix EMBO J 7 1988 2435 2442
8. S. Réty, and J. Sopkova A. Lewit-Bentley The crystal structure of a complex of p11 with the annexin II N-terminal peptide Nat. Struct. Biol. 6 1999 89 95
9. A.R. Nazmi, and G. Ozorowski H. Luecke N-terminal acetylation of annexin A2 is required for S100A10 binding Biol. Chem. 393 2012 1141 1150
10. M. Menke, and M. Ross C. Steinem The molecular arrangement of membrane-bound annexin A2-S100A10 tetramer as revealed by scanning force microscopy ChemBioChem 5 2004 1003 1006
11. M. Menke, V. Gerke, and C. Steinem Phosphatidylserine membrane domain clustering induced by annexin A2/S100A10 heterotetramer Biochemistry 44 2005 15296 15303
12. N.A. Gokhale, and A. Abraham W. Cho Phosphoinositide specificity of and mechanism of lipid domain formation by annexin A2-p11 heterotetramer J. Biol. Chem. 280 2005 42831 42840
13. P. Drücker, and M. Pejic V. Gerke Lipid segregation and membrane budding induced by the peripheral membrane binding protein annexin A2 J. Biol. Chem. 288 2013 24764 24776
14. D.M. Engelman Membranes are more mosaic than fluid Nature 438 2005 578 580
15. L.J. Pike The challenge of lipid rafts J. Lipid Res. 50 Suppl 2009 S323 S328
16. G.L. Nicolson The fluid-mosaic model of membrane structure: still relevant to understanding the structure, function and dynamics of biological membranes after more than 40 years Biochim. Biophys. Acta 1838 2014 1451 1466
17. T.-Y. Wang, and J.R. Silvius Cholesterol does not induce segregation of liquid-ordered domains in bilayers modeling the inner leaflet of the plasma membrane Biophys. J. 81 2001 2762 2773
18. V. Kiessling, C. Wan, and L.K. Tamm Domain coupling in asymmetric lipid bilayers Biochim. Biophys. Acta 1788 2009 64 71
19. E. Delage, and J. Puyaubert E. Ruelland Signal transduction pathways involving phosphatidylinositol 4-phosphate and phosphatidylinositol 4,5-bisphosphate: convergences and divergences among eukaryotic kingdoms Prog. Lipid Res. 52 2013 1 14
20. M. Ross, V. Gerke, and C. Steinem Membrane composition affects the reversibility of annexin A2t binding to solid supported membranes: a QCM study Biochemistry 42 2003 3131 3141
21. J.T. Tran, A. Rosengarth, and H. Luecke Cloning, purification and crystallization of full-length human annexin 2 Acta Crystallogr. Sect. D: Biol. Crystallogr. 58 2002 1854 1857
22. E. Kube, and T. Becker V. Gerke Protein-protein interaction studied by site-directed mutagenesis. Characterization of the annexin II-binding site on p11, a member of the S100 protein family J. Biol. Chem. 267 1992 14175 14182
23. M. Osborn, and N. Johnsson K. Weber The submembranous location of p11 and its interaction with the p36 substrate of pp60 src kinase in situ Exp. Cell Res. 175 1988 81 96
24. V. Gerke, and K. Weber Calcium-dependent conformational changes in the 36-kDa subunit of intestinal protein I related to the cellular 36-kDa target of Rous sarcoma virus tyrosine kinase J. Biol. Chem. 260 1985 1688 1695
25. R. Richter, A. Mukhopadhyay, and A. Brisson Pathways of lipid vesicle deposition on solid surfaces: a combined QCM-D and AFM study Biophys. J. 85 2003 3035 3047
26. R.P. Richter, R. Bérat, and A.R. Brisson Formation of solid-supported lipid bilayers: an integrated view Langmuir 22 2006 3497 3505
27. 2: influence of ionic strength and pH on bilayer formation and membrane organization Langmuir 29 2013 14204 14213
28. G. Sauerbrey Verwendung von Schwingquarzen zur Wägung dünner Schichten und zur Mikrowägung Zeitschrift für Physik A Hadrons and Nuclei 155 1959 206 222
29. M. Rodahl, F. Höök, and B. Kasemo QCM operation in liquids: an explanation of measured variations in frequency and Q factor with liquid conductivity Anal. Chem. 68 1996 2219 2227
30. F. Höök, and M. Rodahl B. Kasemo Energy dissipation kinetics for protein and antibody-antigen adsorption under shear oscillation on a quartz crystal microbalance Langmuir 14 1998 729 734
31. J. Rickert, A. Brecht, and W. Göpel QCM operation in liquids: constant sensitivity during formation of extended protein multilayers by affinity Anal. Chem. 69 1997 1441 1448
32. J. Fatisson, F. Azari, and N. Tufenkji Real-time QCM-D monitoring of cellular responses to different cytomorphic agents Biosens. Bioelectron. 26 2011 3207 3212
33. M. Rodahl, F. Höök, and A. Krozer Quartz crystal microbalance setup for frequency and G-factor measurements in gaseous and liquid environments Rev. Sci. Instrum. 66 1995 3924 3930
34. K. Keiji Kanazawa, and J.G. Gordon Ii The oscillation frequency of a quartz resonator in contact with liquid Anal. Chim. Acta 175 1985 99 105
35. Höök, F. 1997. Development of a novel QCM technique for protein adsorption studies. Dissertation. Department of Biochemistry and Biophysics, Calmers University of Technology and Göteborg University, Göteborg, Sweden.
36. K. Kastl, and M. Ross C. Steinem Kinetics and thermodynamics of annexin A1 binding to solid-supported membranes: a QCM study Biochemistry 41 2002 10087 10094
37. J.N. Weiss The Hill equation revisited: uses and misuses FASEB J. 11 1997 835 841
38. M.I. Stefan, and N. Le Novère Cooperative binding PLOS Comput. Biol. 9 2013 e1003106
39. M.V. Voinova, and M. Rodahl B. Kasemo Viscoelastic acoustic response of layered polymer films at fluid-solid interfaces: Continuum mechanics approach Phys. Scr. 59 1999 391
40. S.J. Martin, V.E. Granstaff, and G.C. Frye Characterization of a quartz crystal microbalance with simultaneous mass and liquid loading Anal. Chem. 63 1991 2272 2281
41. A. Janshoff, H.-J. Galla, and C. Steinem Piezoelectric mass-sensing devices as biosensors-an alternative to optical biosensors? Angew. Chem. Int. Ed. Engl. 39 2000 4004 4032
42. R.E. Weber, and H. Ostojic C. Monge Novel mechanism for high-altitude adaptation in hemoglobin of the Andean frog Telmatobius peruvianus Am. J. Physiol. Regul. Integr. Comp. Physiol. 283 2002 R1052 R1060
43. L. Endrenyi, C. Fajszi, and F.H. Kwong Evaluation of Hill slopes and Hill coefficients when the saturation binding or velocity is not known Eur. J. Biochem. 51 1975 317 328
44. A.K. Thakur, and D. Rodbard Graphical aids to interpretation of Scatchard plots and dose-response curves J. Theor. Biol. 80 1979 383 403
45. G.C. Chamness, and W.L. McGuire Scatchard plots: common errors in correction and interpretation Steroids 26 1975 538 542
46. A.C. Notides, N. Lerner, and D.E. Hamilton Positive cooperativity of the estrogen receptor Proc. Natl. Acad. Sci. USA 78 1981 4926 4930
47. V. Gerke, and S.E. Moss Annexins and membrane dynamics Biochim. Biophys. Acta 1357 1997 129 154
48. D.M. Waisman Annexin II tetramer: structure and function Mol. Cell. Biochem. 149-150 1995 301 322
49. B. Antonny Mechanisms of membrane curvature sensing Annu. Rev. Biochem. 80 2011 101 123
50. A. Rosengarth, V. Gerke, and H. Luecke X-ray structure of full-length annexin 1 and implications for membrane aggregation J. Mol. Biol. 306 2001 489 498
51. 2+ is not required for the association of annexin II with early endosomes J. Cell Sci. 110 1997 221 228
52. K. Simons, and E. Ikonen Functional rafts in cell membranes Nature 387 1997 569 572
53. K. Simons, and D. Toomre Lipid rafts and signal transduction Nat. Rev. Mol. Cell Biol. 1 2000 31 39
54. Z.T. Graber, and Z. Jiang E.E. Kooijman Phosphatidylinositol-4,5-bisphosphate ionization and domain formation in the presence of lipids with hydrogen bond donor capabilities Chem. Phys. Lipids 165 2012 696 704
55. Z.T. Graber, A. Gericke, and E.E. Kooijman Phosphatidylinositol-4,5-bisphosphate ionization in the presence of cholesterol, calcium or magnesium ions Chem. Phys. Lipids 182 2014 62 72
56. 2+)-binding sites in human annexin II Eur. J. Biochem. 207 1992 923 930
57. A. Rosengarth, and H. Luecke Annexin A2. Does it induce membrane aggregation by a new multimeric state of the protein? Annexins 1 2004 129 136
58. M.A. Swairjo, and N.O. Concha B.A. Seaton Ca(2+)-bridging mechanism and phospholipid head group recognition in the membrane-binding protein annexin V Nat. Struct. Biol. 2 1995 968 974
59. F. Höök, and M. Rodahl P. Brzezinski Structural changes in hemoglobin during adsorption to solid surfaces: effects of pH, ionic strength, and ligand binding Proc. Natl. Acad. Sci. USA 95 1998 12271 12276
60. S. Oliferenko, and K. Paiha L.A. Huber Analysis of CD44-containing lipid rafts: Recruitment of annexin II and stabilization by the actin cytoskeleton J. Cell Biol. 146 1999 843 854
61. U. Rescher, and D. Ruhe V. Gerke Annexin 2 is a phosphatidylinositol (4,5)-bisphosphate binding protein recruited to actin assembly sites at cellular membranes J. Cell Sci. 117 2004 3473 3480
62. 2 interaction and phosphorylation Biophys. J. 100 2011 1708 1717
63. M.A. Lemmon, and K.M. Ferguson J. Schlessinger Specific and high-affinity binding of inositol phosphates to an isolated pleckstrin homology domain Proc. Natl. Acad. Sci. USA 92 1995 10472 10476
64. D.E. Klein, and A. Lee M.A. Lemmon The pleckstrin homology domains of dynamin isoforms require oligomerization for high affinity phosphoinositide binding J. Biol. Chem. 273 1998 27725 27733
65. L. M A, and F. M F. K Regulatory recruitment of signalling molecules to the cell membrane by pleckstrin homology domains Trends Cell Biol. 7 1997 237 242
66. S. Chiantia, and E. London Acyl chain length and saturation modulate interleaflet coupling in asymmetric bilayers: effects on dynamics and structural order Biophys. J. 103 2012 2311 2319
67. Q. Lin, and E. London Preparation of artificial plasma membrane mimicking vesicles with lipid asymmetry PLoS ONE 9 2014 e87903
68. S. Chiantia, and P. Schwille E. London Asymmetric GUVs prepared by MβCD-mediated lipid exchange: an FCS study Biophys. J. 100 2011 L1 L3
69. 2+) concentration Biochim. Biophys. Acta 1510 2001 18 28
70. D.S. Drust, and C.E. Creutz Aggregation of chromaffin granules by calpactin at micromolar levels of calcium Nature 331 1988 88 91
71. T.C. Evans Jr., and G.L. Nelsestuen Calcium and membrane-binding properties of monomeric and multimeric annexin II Biochemistry 33 1994 13231 13238
72. L. Liu, A.B. Fisher, and U.-J.P. Zimmerman Lung annexin II promotes fusion of isolated lamellar bodies with liposomes Biochim. Biophys. Acta 1259 1995 166 172
73. R.A. Dick, and S.L. Goh V.M. Vogt HIV-1 Gag protein can sense the cholesterol and acyl chain environment in model membranes Proc. Natl. Acad. Sci. USA 109 2012 18761 18766
74. 2+)-binding sites Biochem. J. 298 1994 553 559
75. Y.-H. Wang, and A. Collins P.A. Janmey Divalent cation-induced cluster formation by polyphosphoinositides in model membranes J. Am. Chem. Soc. 134 2012 3387 3395
76. 2) molar fractions induce nanometer size clustering in giant unilamellar vesicles Chem. Phys. Lipids 177 2014 51 63
77. Z. Jiang, and R.E. Redfern A. Gericke Cholesterol stabilizes fluid phosphoinositide domains Chem. Phys. Lipids 182 2014 52 61
78. C. Janko, and I. Jeremic M. Herrmann Cooperative binding of Annexin A5 to phosphatidylserine on apoptotic cell membranes Phys. Biol. 10 2013 065006