Lipid segregation and membrane budding induced by the peripheral membrane binding protein annexin A2

Journal of Biological Chemistry

Volumn 288, Issue 34, 2013, Pages 24764-24776

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

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDIC PHOSPHOLIPIDS; GIANT UNILAMELLAR VESICLES; MEMBRANE INDENTATION; MEMBRANE TRAFFICKING; MEMBRANE-ASSOCIATED PROTEINS; PHOSPHATIDYLINOSITOL 4 ,5-BISPHOSPHATE; PHOSPHOLIPID BINDING; PLECKSTRIN HOMOLOGY DOMAINS;

ANTIBIOTICS; CELL MEMBRANES; CHOLESTEROL; MEMBRANES; MOLECULAR BIOLOGY; PHASE SEPARATION; PHOSPHOLIPIDS; SIGNAL TRANSDUCTION;

PROTEINS;

LIPOCORTIN 2; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHOLIPASE C DELTA1; PHOSPHOLIPID; PLECKSTRIN; PROTEIN S 100; PROTEIN S 100A10; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; ESCHERICHIA COLI; FLUORESCENCE; LIPID ANALYSIS; LIPID COMPOSITION; LIPID VESICLE; MEMBRANE BIOLOGY; MEMBRANE BUDDING; MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PURIFICATION;

ANNEXIN; CALCIUM; GIANT UNILAMELLAR VESICLES; LIPID RAFT; MEMBRANE BUDDING; MEMBRANE CURVATURE; MEMBRANE STRUCTURE; MICRODOMAIN; PHOSPHATIDYLINOSITOL 4,5-BISPHOSPHATE; PHOSPHOLIPID VESICLE;

ANNEXIN A2; HUMANS; MEMBRANE MICRODOMAINS; MEMBRANES, ARTIFICIAL; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PHOSPHOLIPASE C DELTA; S100 PROTEINS;

EID: 84883178414     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.474023     Document Type: Article

References (58)

1. Zimmerberg, J., and Kozlov, M. M. (2006) How proteins produce cellular membrane curvature. Nat. Rev. Mol. Cell Biol. 7, 9-19
2. Mim, C., and Unger, V. M. (2012) Membrane curvature and its generation by BAR proteins. Trends Biochem. Sci. 37, 526-533
3. Faini, M., Beck, R., Wieland, F. T., and Briggs, J. A. (2013) Vesicle coats. Structure, function, and general principles of assembly. Trends Cell Biol. 23, 279-288
4. Antonny, B. (2011) Mechanisms of membrane curvature sensing. Annu. Rev. Biochem. 80, 101-123
5. Cornell, R. B., and Taneva, S. G. (2006) Amphipathic helices as mediators of the membrane interaction of amphitropic proteins and as modulators of bilayer physical properties. Curr. Protein Pept. Sci. 7, 539-552
6. 2+ signalling to membrane dynamics. Nat. Rev. Mol. Cell Biol. 6, 449-461
7. Gerke, V., and Moss, S. E. (2002) Annexins. From structure to function. Physiol. Rev. 82, 331-371
8. Raynal, P., and Pollard, H. B. (1994) Annexins. The problem of assessing the biological role for a gene family of multifunctional calcium-and phospholipid-binding proteins. Biochim. Biophys. Acta 1197, 63-93
9. Morel, E., and Gruenberg, J. (2007) The p11/S100A10 light chain of annexin A2 is dispensable for annexin A2 association to endosomes and functions in endosomal transport. PLoS ONE 2, e1118
10. 2+-binding sites. J. Cell Sci. 103, 733-742
11. Johnsson N., Marriott, G., and Weber K. (1988) p36, the major cytoplasmic substrate of src tyrosine protein kinase, binds to its p11 regulatory subunit via a short amino-terminal amphipathic helix. EMBO J. 7, 2435-2442
12. Réty, S., Sopkova, J., Renouard, M., Osterloh, D., Gerke, V., Tabaries, S., Russo-Marie, F., and Lewit-Bentley, A. (1999) The crystal structure of a complex of p11 with the annexin II N-terminal peptide. Nat. Struct. Mol. Biol. 6, 89-95
13. Nazmi, A. R., Ozorowski, G., Pejic, M., Whitelegge, J. P., Gerke, V., and Luecke, H. (2012) N-terminal acetylation of annexin A2 is required for S100A10 binding. Biol. Chem. 393, 1141-1150
14. Oliferenko, S., Paiha, K., Harder, T., Gerke, V., Schwärzler, C., Schwarz, H., Beug, H., Günthert, U., and Huber, L. A. (1999) Analysis of Cd44-containing lipid rafts. Recruitment of annexin II and stabilization by the actin cytoskeleton. J. Cell Biol. 146, 843-854
15. Rescher, U., Ruhe, D., Ludwig, C., Zobiack, N., and Gerke, V. (2004) Annexin 2 is a phosphatidylinositol (4,5)-bisphosphate binding protein recruited to actin assembly sites at cellular membranes. J. Cell Sci. 117, 3473-3480
16. Chasserot-Golaz, S., Vitale, N., Umbrecht-Jenck, E., Knight, D., Gerke, V., and Bader, M.-F. (2005) Annexin 2 promotes the formation of lipid microdomains required for calcium-regulated exocytosis of dense-core vesicles. Mol. Biol. Cell 16, 1108-1119
17. Morel, E., Parton, R. G., and Gruenberg, J. (2009) Annexin A2-dependent polymerization of actin mediates endosome biogenesis. Dev. Cell 16, 445-457
18. Menke, M., Ross, M., Gerke, V., and Steinem, C. (2004) The molecular arrangement of membrane-bound annexin A2-S100A10 tetramer as revealed by scanning force microscopy. Chembiochem 5, 1003-1006
19. Menke, M., Gerke, V., and Steinem, C. (2005) Phosphatidylserine membrane domain clustering induced by annexin A2/S100A10 heterotetramer. Biochemistry 44, 15296-15303
20. Gokhale, N. A., Abraham, A., Digman, M. A., Gratton, E., and Cho, W. (2005) Phosphoinositide specificity of and mechanism of lipid domain formation by annexin A2-p11 heterotetramer. J. Biol. Chem. 280, 42831-42840
21. Kiessling, V., Wan, C., and Tamm, L. K. (2009) Domain coupling in asymmetric lipid bilayers. Biochim. Biophys. Acta 1788, 64-71
22. Kiessling, V., Crane, J. M., and Tamm, L. K. (2006) Transbilayer effects of raft-like lipid domains in asymmetric planar bilayers measured by single molecule tracking. Biophys. J. 91, 3313-3326
23. Lingwood, D., and Simons, K. (2010) Lipid rafts as a membrane-organizing principle. Science 327, 46-50
24. Lambert, O., Gerke, V., Bader, M.-F., Porte, F., and Brisson, A. (1997) Structural analysis of junctions formed between lipid membranes and several annexins by cryo-electron microscopy. J. Mol. Biol. 272, 42-55
25. Lambert, O., Cavusoglu, N., Gallay, J., Vincent, M., Rigaud, J. L., Henry, J.-P., and Ayala-Sanmartin, J. (2004) Novel organization and properties of annexin 2-membrane complexes. J. Biol. Chem. 279, 10872-10882
26. Drust, D. S., and Creutz, C. E. (1988) Aggregation of chromaffin granules by calpactin at micromolar levels of calcium. Nature 331, 88-91
27. Osborn, M., Johnsson, N., Wehland, J., and Weber, K. (1988) The submembranous location of p11 and its interaction with the p36 substrate of pp60 src kinase in situ. Exp. Cell Res. 175, 81-96
28. Tran, J. T., Rosengarth, A., and Luecke, H. (2002) Cloning, purification, and crystallization of full-length human annexin 2. Acta Crystallogr. D Biol. Crystallogr. 58, 1854-1857
29. 2+-binding site in human annexin II by site-directed mutagenesis. J. Biol. Chem. 266, 14732-14739
30. Kube, E., Becker, T., Weber, K., and Gerke, V. (1992) 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, 14175-14182
31. König, J., Prenen, J., Nilius, B., and Gerke, V. (1998) The annexin II-p11 complex is involved in regulated exocytosis in bovine pulmonary artery endothelial cells. J. Biol. Chem. 273, 19679-19684
32. Gerke, V., and Weber, K. (1985) 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, 1688-1695
33. Ross, M., Gerke, V., and Steinem, C. (2003) Membrane composition affects the reversibility of annexin A2t binding to solid supported membranes. A QCM study. Biochemistry 42, 3131-3141
34. Angelova, M. I., and Dimitrov, D. S. (1986) Liposome electroformation. Faraday Discuss. Chem. Soc. 81, 303-311
35. Kauscher, U., Stuart, M. C., Drücker, P., Galla, H.-J., and Ravoo, B. J. (2013) Incorporation of amphiphilic cyclodextrins into liposomes as artificial receptor units. Langmuir 29, 7377-7383
36. Horger, K. S., Estes, D. J., Capone, R., and Mayer, M. (2009) Films of agarose enable rapid formation of giant liposomes in solutions of physiologic ionic strength. J. Am. Chem. Soc. 131, 1810-1819
37. Rosengarth, A., and Luecke, H. (2004) Annexin A2. Does it induce membrane aggregation by a new multimeric state of the protein? Annexins 1, 129-136
38. Johnsson, N., and Weber, K. (1990) Alkylation of cysteine 82 of p11 abolishes the complex formation with the tyrosine-protein kinase substrate p36 (annexin 2, calpactin 1, lipocortin 2). J. Biol. Chem. 265, 14464-14468
39. van Meer, G., Voelker, D. R., and Feigenson, G. W. (2008) Membrane lipids. Where they are and how they behave. Nat. Rev. Mol. Cell Biol. 9, 112-124
40. Morales-Penningston, N. F., Wu, J., Farkas, E. R., Goh, S. L., Konyakhina, T. M., Zheng, J. Y., Webb, W. W., and Feigenson, G. W. (2010) GUV preparation and imaging. Minimizing artifacts. Biochim. Biophys. Acta 1798, 1324-1332
41. Juhasz, J., Davis, J. H., and Sharom, F. J. (2012) Fluorescent probe partitioning in GUVs of binary phospholipid mixtures. Implications for interpreting phase behavior. Biochim. Biophys. Acta 1818, 19-26
42. Baumgart, T., Hunt, G., Farkas, E. R., Webb, W. W., and Feigenson, G. W. (2007) Fluorescence probe partitioning between Lo/Ld phases in lipid membranes. Biochim. Biophys. Acta 1768, 2182-2194
43. Rosengarth, A., Gerke, V., and Luecke, H. (2001) X-ray structure of fulllength annexin 1 and implications for membrane aggregation. J. Mol. Biol. 306, 489-498
44. 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. (2004) Annexin 2 binding to phosphatidylinositol 4,5-bisphosphate on endocytic vesicles is regulated by the stress response pathway. J. Biol. Chem. 279, 14157-14164
45. Levental, I., Grzybek, M., and Simons, K. (2011) Raft domains of variable properties and compositions in plasma membrane vesicles. Proc. Natl. Acad. Sci. 108, 11411-11416
46. Powell, M. A., and Glenney, J. R. (1987) Regulation of calpactin I phospholipid binding by calpactin I light-chain binding and phosphorylation by p60v-src. Biochem. J. 247, 321-328
47. Zobiack, N., Rescher, U., Laarmann, S., Michgehl, S., Schmidt, M. A., and Gerke, V. (2002) Cell-surface attachment of pedestal-forming enteropathogenic E. coli induces a clustering of raft components and a recruitment of annexin 2. J. Cell Sci. 115, 91-98
48. Rossman, J. S., Jing, X., Leser, G. P., and Lamb, R. A. (2010) Influenza virus M2 protein mediates ESCRT-independent membrane scission. Cell 142, 902-913
49. Gruenberg, J., and Emans, N. (1993) Annexins in membrane traffic. Trends Cell Biol. 3, 224-227
50. Harder, T., and Gerke, V. (1993) The subcellular distribution of early endosomes is affected by the annexin II2p11(2) complex. J. Cell Biol. 123, 1119-1132
51. Zobiack, N., Rescher, U., Ludwig, C., Zeuschner, D., and Gerke, V. (2003) The annexin 2/S100A10 complex controls the distribution of transferrin receptor-containing recycling endosomes. Mol. Biol. Cell 14, 4896-4908
52. Mayran, N., Parton, R. G., and Gruenberg, J. (2003) Annexin II regulates multivesicular endosome biogenesis in the degradation pathway of animal cells. EMBO J. 22, 3242-3253
53. White, I. J., Bailey, L. M., Aghakhani, M. R., Moss, S. E., and Futter, C. E. (2006) EGF stimulates annexin 1-dependent inward vesiculation in a multivesicular endosome subpopulation. EMBO J. 25, 1-12
54. Harrist, A. V., Ryzhova, E. V., Harvey, T., and González-Scarano, F. (2009) Anx2 interacts with HIV-1 Gag at phosphatidylinositol (4,5) bisphosphate-containing lipid rafts and increases viral production in 293T cells. PLoS ONE 4, e5020
55. Sandvig, K., and Llorente, A. (2012) Proteomic analysis of microvesicles released by the human prostate cancer cell line PC-3. Mol. Cell. Proteomics 11, doi 10.1074/mcp.M111.012914
56. Draeger, A., Monastyrskaya, K., Burkhard, F. C., Wobus, A. M., Moss, S. E., and Babiychuk, E. B. (2003) Membrane segregation and downregulation of raft markers during sarcolemmal differentiation in skeletal muscle cells. Dev. Biol. 262, 324-334
57. Gillette, J. M., and Nielsen-Preiss, S. M. (2004) The role of annexin 2 in osteoblastic mineralization. J. Cell Sci. 117, 441-449
58. Rescher, U., and Gerke, V. (2008) S100A10/p11. Family, friends, and functions. Pflugers Arch. 455, 575-582