Organization and synergistic binding of copine I and annexin A1 on supported lipid bilayers observed by atomic force microscopy

Biochimica et Biophysica Acta - Biomembranes

Volumn 1788, Issue 9, 2009, Pages 1950-1961

  Creutz, Carl E ^a   Edwardson, J Michael ^b  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Annexin; Atomic force microscopy; Copine; Lipid domain; Supported bilayer

Indexed keywords

BINDING PROTEIN; CALCIUM ION; COPINE 1; DIOLEOYLPHOSPHATIDYLCHOLINE; LIPOCORTIN 1; PHOSPHATIDYLSERINE; UNCLASSIFIED DRUG;

ARTICLE; ATOMIC FORCE MICROSCOPY; CONTROLLED STUDY; HUMAN; IN VITRO STUDY; LIPID BILAYER; MEMBRANE STRUCTURE; MONITORING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION;

ANNEXIN A1; CARRIER PROTEINS; HUMANS; LIPID BILAYERS; MICROSCOPY, ATOMIC FORCE; PHOSPHATIDYLSERINES;

EID: 68749117644     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2009.06.009     Document Type: Article

References (46)

1. Creutz C.E., Pazoles C.J., and Pollard H.B. Identification and purification of an adrenal medullary protein (synexin) that causes calcium dependent aggregation of isolated chromaffin granules. J. Biol. Chem. 253 (1978) 2858-2866
2. Creutz C.E. The annexins and exocytosis. Science 258 (1992) 924-931
3. 2+ signalling to membrane dynamics. Nat. Rev., Mol. Cell Biol. 6 (2005) 449-461
4. Creutz C.E., Tomsig J.L., Snyder S.L., Skouri F., Beisson J., and Cohen J. The copines: a novel class of C2 domain-containing, calcium-dependent, phospholipid-binding proteins conserved from Paramecium to humans. J. Biol. Chem. 273 (1998) 1393-1402
5. Tomsig J.L., Snyder S.L., and Creutz C.E. Identification of targets for calcium signalling through the copine family of proteins: characterization of a coiled-coil copine-binding motif. J. Biol. Chem. 278 (2003) 10048-10054
6. Tomsig J.L., and Creutz C.E. Copines: a ubiquitous family of calcium-dependent, phospholipid-binding proteins. Cell. Mol. Life Sci. 59 (2002) 1467-1477
7. Creutz C.E., and Snyder S.L. Interactions of annexins with the μ subunits of the clathrin assembly proteins. Biochemistry 44 (2005) 13795-13806
8. Lee J.O., Rieu P., Arnaout M.A., and Liddington R. Crystal structure of the A domain from the alpha subunit of integrin CR3 (CD11b/CD18). Cell 80 (1995) 631-638
9. Tomsig J.L., Sohma H., and Creutz C.E. Calcium-dependent regulation of tumour necrosis factor-alpha receptor signalling by copine. Biochem J. 378 (2004) 1089-1094
10. Kretsinger R.H., and Creutz C.E. Consensus in exocytosis. Nature 320 (1986) 573
11. Hinderliter A.K., Almeida P.F.F., Biltonen R.L., and Creutz C.E. Membrane domain formation by calcium-dependent, lipid-binding proteins: insights from the C2 motif. Biochim. Biophys. Acta 1448 (1998) 227-235
12. Babiychuk E.B., and Draeger A. Annexins in cell membrane dynamics, Ca(2+)-regulated association of lipid microdomains. J. Cell Biol. 150 (2000) 1113-1124
13. Draeger A., Wray S., and Babiychuk E.B. Domain architecture of the smooth-muscle plasma membrane: regulation by annexins. Biochem. J. 387 (2005) 309-314
14. Creutz C.E., Kambouris N.G., Snyder S.L., Hamman H.C., Nelson M.R., Liu W., and Rock P. Effects of the expression of mammalian annexins in yeast secretory mutants. J. Cell Sci. 103 (1992) 1177-1192
15. Brian A.A., and McConnell H.M. Allogenic stimulation of cytotoxic T cells by supported planar membranes. Proc. Natl. Acad. Sci U. S. A. 81 (1984) 6159-6163
16. Mou J., Yang J., and Shao Z. Tris(hydroxymethyl)aminomethane induced a ripple phase in supported unilamellar phospholipid bilayers. Biochemistry 33 (1994) 4439-4443
17. Shahin V., Datta D., Hui E., Henderson R.M., Chapman E.R., and Edwardson J.M. Synaptotagmin perturbs the structure of phospholipid bilayers. Biochemistry 47 (2008) 2143-2152
18. Tomsig J.L., and Creutz C.E. Biochemical characterization of copine: a ubiquitous calcium-dependent, phospholipid-binding protein. Biochemistry 39 (2000) 16163-16175
19. Schneider S.W., Lärmer J., Henderson R.M., and Oberleithner H. Molecular weights of individual proteins correlate with molecular volumes measured by atomic force microscopy. Pfluegers Arch. 435 (1998) 362-367
20. Herrick D.Z., Sterbling S., Rasch K.A., Hinderliter A., and Cafiso D.S. Position of synaptotagmin I at the membrane interface: cooperative interactions of tandem C2 domains. Biochemistry 45 (2006) 9668-9674
21. Ross M., Steinem C., Galla H.J., and Janshoff A. Visualization of chemical and physical properties of calcium-induced domains in DPPC/DPPS Langmuir-Blodgett layers. Langmuir 17 (2001) 2437-2445
22. Menke M., Gerke V., and Steinem C. Phosphatidylserine membrane domain clustering induced by annexin A2/S100A10 heterotetramer. Biochemistry 44 (2005) 15296-15303
23. Richter R.P., and Brisson A.R. Following the formation of supported lipid bilayers on mica: a study combining AFM, QCM-D, and ellipsometry. Biophys. J. 88 (2005) 3422-3433
24. Muller D.J. AFM: a nanotool in membrane biology. Biochemistry 47 (2008) 7986-7998
25. Tokumasu F., Jin A.J., Feigenson G.W., and Dvorak J.A. Nanoscopic lipid domain dynamics revealed by atomic force microscopy. Biophys. J. 84 (2003) 2609-2618
26. Rinia H.A., Snel M.M.E., van der Eerden J.P.J.M., and de Kruijff B. Visualizing detergent resistant domains in model membranes with atomic force microscopy. FEBS Lett. 501 (2001) 92-96
27. Blanchette C.D., Orme C.A., Ratto T.V., and Longo M.L. Quantifying growth of symmetric and asymmetric lipid bilayer domains. Langmuir 24 (2008) 1219-1224
28. Johnston I., and Johnston L.J. Sphingomyelinase generation of ceramide promotes clustering of nanoscale domains in supported bilayer membranes. Biochim. Biophys. Acta 1778 (2008) 185-197
29. Shaw J.E., Epand R.F., Hsu J.C.Y., Mo G.C.H., Epand R.M., and Yip C.M. Cationic peptide-induced remodeling of model membranes: direct visualization by in situ atomic force microscopy. J. Struct. Biol. 162 (2008) 121-138
30. Garcia R., Magerle R., and Perez R. Nanoscale compositional mapping with gentle forces. Nat. Mater. 6 (2007) 405-411
31. Patel D.R., Jao C.C., Mailliard W.S., Isas J.M., Langen R., and Haigler H.T. Calcium-dependent binding of annexin 12 to phospholipid bilayers: stoichiometry and implications. Biochemistry 40 (2001) 7054-7060
32. Fischer T., Lu L., Haigler H.T., and Langen R. Annexin B12 is a sensor of membrane curvature and undergoes major curvature-dependent structural changes. J. Biol. Chem. 282 (2007) 9996-10004
33. Oreopoulos J., and Yip C.M. Probing membrane order and topography in supported lipid bilayers by combined polarized total internal reflection fluorescence-atomic force microscopy. Biophys. J. 96 (2009) 1970-1984
34. J. Oreopoulos, C.M. Yip, Combinatorial microscopy for the study of protein-membrane interactions in supported lipid bilayers: order parameter measurements by combined polarized TIRFM/AFM, J. Struct. Biol. in press, doi:10.1016/j.jsb.2009.02.011.
35. Janshoff A., Ross M., Gerke V., and Steinem C. Visualization of annexin I binding to calcium-induced phosphatidylserine domains. Chembiochem 2 (2001) 587-590
36. Lu Y., Bazzi M.D., and Nelsestuen G.L. Kinetics of annexin VI, calcium, and phospholipid association and dissociation. Biochemistry 34 (1995) 10777-10785
37. Hayes M.J., Merrifield C.J., Shao D., Ayala-Sanmartin J., Schorey C.D., Levine T.P., Proust J., Curran J., Bailly M., and Moss S.E. Annexin 2 binding to phosphatidylinositol 4,5-bisphosphate on endocytic vesicles is regulated by the stress response pathway. J. Biol. Chem. 279 (2004) 14157-14164
38. Babiychuk E.B., Monastyrskaya K., and Draeger A. Fluorescent annexin A1 reveals dynamics of ceramide platforms in living cells. Traffic 9 (2008) 1757-1775
39. Harder T., Kellner R., Parton R.G., and Gruenberg J. Specific release of membrane-bound annexin II and cortical cytoskeletal elements by sequestration of membrane cholesterol. Mol. Biol. Cell 8 (1997) 533-545
40. Zeuschner D., Stoorvogel W., and Gerke V. Association of annexin 2 with recycling endosomes requires either calcium- or cholesterol-stabilized membrane domains. Eur. J. Cell Biol. 80 (2001) 499-507
41. Kastl K., Ross M., Gerke V., and Steinem C. Kinetics and thermodynamics of annexin A1 binding to solid-supported membranes: a QCM study. Biochemistry 41 (2002) 10087-10094
42. Crane J.M., Kiessling V., and Tamm L.K. Measuring lipid asymmetry in planar supported bilayers by fluorescence interference contrast microscopy. Langmuir 21 (2005) 1377-1388
43. Kiessling V., Crane J.M., and Tamm L.K. Transbilayer effects of raft-like lipid domains in asymmetric planar bilayers measured by single molecule tracking. Biophys. J. 91 (2006) 3313-3326
44. Kiessling V., Wan C., and Tamm L.K. Domain coupling in asymmetric lipid bilayers. Biochem. Biophys. Acta 1788 (2009) 64-71
45. Faiss S., Katl K., Janshoff A., and Steinem C. Formation of irreversibly bound annexin A1 protein domains on POPC/POPS solid supported membranes. Biochim. Biophys. Acta 1778 (2008) 1601-1610
46. Richter R.P., Him J.L., Tessier B., Tessier C., and Brisson A.R. On the kinetics of adsorption and two-dimensional self-assembly of annexin A5 on supported lipid bilayers. Biophys. J. 89 (2005) 3372-3385