Annexin A6-Linking Ca2+ signaling with cholesterol transport

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1813, Issue 5, 2011, Pages 935-947

  Enrich, Carlos ^a   Rentero, Carles ^a   de Muga, Sandra Vilà ^a   Reverter, Meritxell ^a   Mulay, Vishwaroop ^b   Wood, Peta ^b   Koese, Meryem ^b   Grewal, Thomas ^b  

^a UNIVERSITY OF BARCELONA   (Spain)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Actin; Annexin A6; Caveolae; Caveolin 1; Cholesterol; PKC?; Ras MAPK

Indexed keywords

ACTIN; CALCIUM ION; CALPHOBINDIN II; CAVEOLIN; CHOLESTEROL; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOLIPASE A2; PROTEIN KINASE C; PROTEIN P120; RAS PROTEIN; SCAFFOLD PROTEIN; VASCULOTROPIN;

ANIMAL CELL; CALCIUM SIGNALING; CELL MEMBRANE; CELL MIGRATION; CELL SURFACE; CELLULAR DISTRIBUTION; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; CYTOPLASM; ENDOCYTOSIS; ENDOSOME; ENZYME ACTIVITY; EXOCYTOSIS; GOLGI COMPLEX; HUMAN; HUMAN CELL; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION;

EID: 79955669430     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2010.09.015     Document Type: Review

References (185)

1. Moss S.E., Morgan R.O. The annexins. Genome Biol. 2004, 5:219.
2. Gerke V., Creutz C.E., Moss S.E. Annexins: linking Ca2+ signalling to membrane dynamics. Nat. Rev. Mol. Cell Biol. 2005, 6:449-461.
3. Bandorowicz-Pikula J. Annexins: Biological Importance and Annexin-Related Pathologies 2005, Landes Bioscience. Kluwer Academic/Plenum Publishers, New York.
4. Benz J., Bergner A., Hofmann A., Demange P., Gottig P., Liemann S., Huber R., Voges D. The structure of recombinant human annexin VI in crystals and membrane-bound. J. Mol. Biol. 1996, 260:638-643.
5. Avila-Sakar A.J., Creutz C.E., Kretsinger R.H. Crystal structure of bovine annexin VI in a calcium-bound state. Biochim. Biophys. Acta 1998, 1387:103-116.
6. Avila-Sakar A.J., Kretsinger R.H., Creutz C.E. Membrane-bound 3D structures reveal the intrinsic flexibility of annexin VI. J. Struct. Biol. 2000, 130:54-62.
7. Buzhynskyy N., Golczak M., Lai-Kee-Him J., Lambert O., Tessier B., Gounou C., Berat R., Simon A., Granier T., Chevalier J.M., Mazeres S., Bandorowicz-Pikula J., Pikula S., Brisson A.R. Annexin-A6 presents two modes of association with phospholipid membranes. A combined QCM-D, AFM and cryo-TEM study. J. Struct. Biol. 2009, 168:107-116.
8. Edwards H.C., Crumpton M.J. Ca(2+)-dependent phospholipid and arachidonic acid binding by the placental annexins VI and IV. Eur. J. Biochem. 1991, 198:121-129.
9. Grewal T., Koese M., Rentero C., Enrich C. Annexin A6-regulator of the EGFR/Ras signalling pathway and cholesterol homeostasis. Int. J. Biochem. Cell Biol. 2010, 42:580-584.
10. Sztolsztener M.E., Strzelecka-Kiliszek A., Pikula S., Tylki-Szymanska A., Bandorowicz-Pikula J. Cholesterol as a factor regulating intracellular localization of annexin A6 in Niemann-Pick type C human skin fibroblasts. Arch. Biochem. Biophys. 2010, 493:221-233.
11. Domon M.M., Matar G., Strzelecka-Kiliszek A., Bandorowicz-Pikula J., Pikula S., Besson F. Interaction of annexin A6 with cholesterol rich membranes is pH-dependent and mediated by the sterol OH. J. Colloid Interface Sci. 2010, 346:436-441.
12. Golczak M., Kirilenko A., Bandorowicz-Pikula J., Desbat B., Pikula S. Structure of human annexin a6 at the air-water interface and in a membrane-bound state. Biophys. J. 2004, 87:1215-1226.
13. de Diego I., Schwartz F., Siegfried H., Dauterstedt P., Heeren J., Beisiegel U., Enrich C., Grewal T. Cholesterol modulates the membrane binding and intracellular distribution of annexin 6. J. Biol. Chem. 2002, 277:32187-32194.
14. Grewal T., Heeren J., Mewawala D., Schnitgerhans T., Wendt D., Salomon G., Enrich C., Beisiegel U., Jackle S. Annexin VI stimulates endocytosis and is involved in the trafficking of low density lipoprotein to the prelysosomal compartment. J. Biol. Chem. 2000, 275:33806-33813.
15. Simons K., Ikonen E. How cells handle cholesterol. Science 2000, 290:1721-1726.
16. Lippincott-Schwartz J., Phair R.D. Lipids and cholesterol as regulators of traffic in the endomembrane system. Annu. Rev. Biophys. 2010, 39:559-578.
17. Ayala-Sanmartin J. Cholesterol enhances phospholipid binding and aggregation of annexins by their core domain. Biochem. Biophys. Res. Commun. 2001, 283:72-79.
18. Ayala-Sanmartin J., Henry J.P., Pradel L.A. Cholesterol regulates membrane binding and aggregation by annexin 2 at submicromolar Ca(2+) concentration. Biochim. Biophys. Acta 2001, 1510:18-28.
19. Smart E.J., De Rose R.A., Farber S.A. Annexin 2-caveolin 1 complex is a target of ezetimibe and regulates intestinal cholesterol transport. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:3450-3455.
20. Uittenbogaard A., Everson W.V., Matveev S.V., Smart E.J. Cholesteryl ester is transported from caveolae to internal membranes as part of a caveolin-annexin II lipid-protein complex. J. Biol. Chem. 2002, 277:4925-4931.
21. Mayran N., Parton R.G., Gruenberg J. Annexin II regulates multivesicular endosome biogenesis in the degradation pathway of animal cells. EMBO J. 2003, 22:3242-3253.
22. Monastyrskaya K., Babiychuk E.B., Draeger A. The annexins: spatial and temporal coordination of signaling events during cellular stress. Cell. Mol. Life Sci. 2009, 66:2623-2642.
23. Golczak M., Kirilenko A., Bandorowicz-Pikula J., Pikula S. Conformational states of annexin VI in solution induced by acidic pH. FEBS Lett. 2001, 496:49-54.
24. Golczak M., Kirilenko A., Bandorowicz-Pikula J., Pikula S. N- and C-terminal halves of human annexin VI differ in ability to form low pH-induced ion channels. Biochem. Biophys. Res. Commun. 2001, 284:785-791.
25. Monastyrskaya K., Tschumi F., Babiychuk E.B., Stroka D., Draeger A. Annexins sense changes in intracellular pH during hypoxia. Biochem. J. 2008, 409:65-75.
26. Cubells L., Vila de Muga S., Tebar F., Wood P., Evans R., Ingelmo-Torres M., Calvo M., Gaus K., Pol A., Grewal T., Enrich C. Annexin A6-induced alterations in cholesterol transport and caveolin export from the Golgi complex. Traffic 2007, 8:1568-1589.
27. Mobius W., van Donselaar E., Ohno-Iwashita Y., Shimada Y., Heijnen H.F., Slot J.W., Geuze H.J. Recycling compartments and the internal vesicles of multivesicular bodies harbor most of the cholesterol found in the endocytic pathway. Traffic 2003, 4:222-231.
28. Goldstein J.L., Brown M.S. Lipoprotein receptors and the control of plasma LDL cholesterol levels. Eur. Heart J. 1992, 13:34-36.
29. Brown M.S., Goldstein J.L. A proteolytic pathway that controls the cholesterol content of membranes, cells, and blood. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:11041-11048.
30. Pol A., Luetterforst R., Lindsay M., Heino S., Ikonen E., Parton R.G. A caveolin dominant negative mutant associates with lipid bodies and induces intracellular cholesterol imbalance. J. Cell Biol. 2001, 152:1057-1070.
31. Roy S., Luetterforst R., Harding A., Apolloni A., Etheridge M., Stang E., Rolls B., Hancock J.F., Parton R.G. Dominant-negative caveolin inhibits H-Ras function by disrupting cholesterol-rich plasma membrane domains. Nat. Cell Biol. 1999, 1:98-105.
32. Pons M., Tebar F., Kirchhoff M., Peiro S., de Diego I., Grewal T., Enrich C. Activation of Raf-1 is defective in annexin 6 overexpressing Chinese hamster ovary cells. FEBS Lett. 2001, 501:69-73.
33. Grewal T., de Diego I., Kirchhoff M.F., Tebar F., Heeren J., Rinninger F., Enrich C. High density lipoprotein-induced signaling of the MAPK pathway involves scavenger receptor type BI-mediated activation of Ras. J. Biol. Chem. 2003, 278:16478-16481.
34. Rentero C., Evans R., Wood P., Tebar F., Vila de Muga S., Cubells L., de Diego I., Hayes T.E., Hughes W.E., Pol A., Rye K.A., Enrich C., Grewal T. Inhibition of H-Ras and MAPK is compensated by PKC-dependent pathways in annexin A6 expressing cells. Cell. Signal. 2006, 18:1006-1016.
35. Grewal T., Evans R., Rentero C., Tebar F., Cubells L., de Diego I., Kirchhoff M.F., Hughes W.E., Heeren J., Rye K.A., Rinninger F., Daly R.J., Pol A., Enrich C. Annexin A6 stimulates the membrane recruitment of p120GAP to modulate Ras and Raf-1 activity. Oncogene 2005, 24:5809-5820.
36. Theobald J., Hanby A., Patel K., Moss S.E. Annexin VI has tumour-suppressor activity in human A431 squamous epithelial carcinoma cells. Br. J. Cancer 1995, 71:786-788.
37. Theobald J., Smith P.D., Jacob S.M., Moss S.E. Expression of annexin VI in A431 carcinoma cells suppresses proliferation: a possible role for annexin VI in cell growth regulation. Biochim. Biophys. Acta 1994, 1223:383-390.
38. Vila de Muga S., Timpson P., Cubells L., Evans R., Hayes T.E., Rentero C., Hegemann A., Reverter M., Leschner J., Pol A., Tebar F., Daly R.J., Enrich C., Grewal T. Annexin A6 inhibits Ras signalling in breast cancer cells. Oncogene 2009, 28:363-377.
39. Ikonen E., Parton R.G. Caveolins and cellular cholesterol balance. Traffic 2000, 1:212-217.
40. Garver W.S., Krishnan K., Gallagos J.R., Michikawa M., Francis G.A., Heidenreich R.A. Niemann-Pick C1 protein regulates cholesterol transport to the trans-Golgi network and plasma membrane caveolae. J. Lipid Res. 2002, 43:579-589.
41. te Vruchte D., Lloyd-Evans E., Veldman R.J., Neville D.C., Dwek R.A., Platt F.M., van Blitterswijk W.J., Sillence D.J. Accumulation of glycosphingolipids in Niemann-Pick C disease disrupts endosomal transport. J. Biol. Chem. 2004, 279:26167-26175.
42. Babiychuk E.B., Draeger A. Annexins in cell membrane dynamics. Ca(2+)-regulated association of lipid microdomains. J. Cell Biol. 2000, 150:1113-1124.
43. Orito A., Kumanogoh H., Yasaka K., Sokawa J., Hidaka H., Sokawa Y., Maekawa S. Calcium-dependent association of annexin VI, protein kinase C alpha, and neurocalcin alpha on the raft fraction derived from the synaptic plasma membrane of rat brain. J. Neurosci. Res. 2001, 64:235-241.
44. Le Lay S., Li Q., Proschogo N., Rodriguez M., Gunaratnam K., Cartland S., Rentero C., Jessup W., Mitchell T., Gaus K. Caveolin-1-dependent and -independent membrane domains. J. Lipid Res. 2009, 50:1609-1620.
45. Brown W.J., Chambers K., Doody A. Phospholipase A2 (PLA2) enzymes in membrane trafficking: mediators of membrane shape and function. Traffic 2003, 4:214-221.
46. Niknami M., Patel M., Witting P.K., Dong Q. Molecules in focus: cytosolic phospholipase A2-alpha. Int. J. Biochem. Cell Biol. 2009, 41:994-997.
47. San Pietro E., Capestrano M., Polishchuk E.V., DiPentima A., Trucco A., Zizza P., Mariggio S., Pulvirenti T., Sallese M., Tete S., Mironov A.A., Leslie C.C., Corda D., Luini A., Polishchuk R.S. Group IV phospholipase A(2)alpha controls the formation of inter-cisternal continuities involved in intra-Golgi transport. PLoS Biol. 2009, 7:e1000194.
48. Grimmer S., Ying M., Walchli S., van Deurs B., Sandvig K. Golgi vesiculation induced by cholesterol occurs by a dynamin- and cPLA2-dependent mechanism. Traffic 2005, 6:144-156.
49. Klapisz E., Masliah J., Bereziat G., Wolf C., Koumanov K.S. Sphingolipids and cholesterol modulate membrane susceptibility to cytosolic phospholipase A(2). J. Lipid Res. 2000, 41:1680-1688.
50. Cubells L., de Muga S.V., Tebar F., Bonventre J.V., Balsinde J., Pol A., Grewal T., Enrich C. Annexin A6-induced inhibition of cytoplasmic phospholipase A2 is linked to caveolin-1 export from the Golgi. J. Biol. Chem. 2008, 283:10174-10183.
51. Maxfield F.R., Wustner D. Intracellular cholesterol transport. J. Clin. Invest. 2002, 110:891-898.
52. Sudhof T.C., Rothman J.E. Membrane fusion: grappling with SNARE and SM proteins. Science 2009, 323:474-477.
53. Rickman C., Davletov B. Arachidonic acid allows SNARE complex formation in the presence of Munc18. Chem. Biol. 2005, 12:545-553.
54. Darios F., Connell E., Davletov B. Phospholipases and fatty acid signalling in exocytosis. J. Physiol. 2007, 585:699-704.
55. Connell E., Darios F., Broersen K., Gatsby N., Peak-Chew S.Y., Rickman C., Davletov B. Mechanism of arachidonic acid action on syntaxin-Munc18. EMBO Rep. 2007, 8:414-419.
56. Predescu S.A., Predescu D.N., Shimizu K., Klein I.K., Malik A.B. Cholesterol-dependent syntaxin-4 and SNAP-23 clustering regulates caveolar fusion with the endothelial plasma membrane. J. Biol. Chem. 2005, 280:37130-37138.
57. Urano Y., Watanabe H., Murphy S.R., Shibuya Y., Geng Y., Peden A.A., Chang C.C., Chang T.Y. Transport of LDL-derived cholesterol from the NPC1 compartment to the ER involves the trans-Golgi network and the SNARE protein complex. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:16513-16518.
58. Choudhury A., Marks D.L., Proctor K.M., Gould G.W., Pagano R.E. Regulation of caveolar endocytosis by syntaxin 6-dependent delivery of membrane components to the cell surface. Nat. Cell Biol. 2006, 8:317-328.
59. E. Umbrecht-Jenck, V. Demais, V. Calco, Y. Bailly, M.F. Bader, S. Chasserot-Golaz, S100A10-mediated translocation of annexin-A2 to SNARE proteins in adrenergic chromaffin cells undergoing exocytosis. Traffic 11 (2010) 958-971.
60. Solito E., Raguenes-Nicol C., de Coupade C., Bisagni-Faure A., Russo-Marie F. U937 cells deprived of endogenous annexin 1 demonstrate an increased PLA2 activity. Br. J. Pharmacol. 1998, 124:1675-1683.
61. Buckland A.G., Wilton D.C. Inhibition of human cytosolic phospholipase A2 by human annexin V. Biochem. J. 1998, 329:369-372.
62. Nakatani Y., Tanioka T., Sunaga S., Murakami M., Kudo I. Identification of a cellular protein that functionally interacts with the C2 domain of cytosolic phospholipase A(2)alpha. J. Biol. Chem. 2000, 275:1161-1168.
63. Sheridan A.M., Force T., Yoon H.J., O'Leary E., Choukroun G., Taheri M.R., Bonventre J.V. PLIP, a novel splice variant of Tip60, interacts with group IV cytosolic phospholipase A(2), induces apoptosis, and potentiates prostaglandin production. Mol. Cell. Biol. 2001, 21:4470-4481.
64. Moes M., Boonstra J., Regan-Klapisz E. Novel role of cPLA(2)alpha in membrane and actin dynamics. Cell. Mol. Life Sci. 2010, 67:1547-1557.
65. Lin L.L., Wartmann M., Lin A.Y., Knopf J.L., Seth A., Davis R.J. cPLA2 is phosphorylated and activated by MAP kinase. Cell 1993, 72:269-278.
66. Gijon M.A., Spencer D.M., Siddiqi A.R., Bonventre J.V., Leslie C.C. Cytosolic phospholipase A2 is required for macrophage arachidonic acid release by agonists that Do and Do not mobilize calcium. Novel role of mitogen-activated protein kinase pathways in cytosolic phospholipase A2 regulation. J. Biol. Chem. 2000, 275:20146-20156.
67. Boonstra J., van Rossum G.S. The role of cytosolic phospholipase A2 in cell cycle progression. Prog. Cell Cycle Res. 2003, 5:181-190.
68. Clark J.D., Lin L.L., Kriz R.W., Ramesha C.S., Sultzman L.A., Lin A.Y., Milona N., Knopf J.L. A novel arachidonic acid-selective cytosolic PLA2 contains a Ca(2+)-dependent translocation domain with homology to PKC and GAP. Cell 1991, 65:1043-1051.
69. Zhou L., Choi H.Y., Li W.P., Xu F., Herz J. LRP1 controls cPLA2 phosphorylation, ABCA1 expression and cellular cholesterol export. PLoS One 2009, 4:e6853.
70. Grewal T., Enrich C. Annexins-modulators of EGF receptor signalling and trafficking. Cell. Signal. 2009, 21:847-858.
71. Grewal T., Enrich C. Molecular mechanisms involved in Ras inactivation: the annexin A6-p120GAP complex. Bioessays 2006, 28:1211-1220.
72. Creutz C.E., Snyder S.L. Interactions of annexins with the mu subunits of the clathrin assembly proteins. Biochemistry 2005, 44:13795-13806.
73. Calvo M., Enrich C. Biochemical analysis of a caveolae-enriched plasma membrane fraction from rat liver. Electrophoresis 2000, 21:3386-3395.
74. Pol A., Ortega D., Enrich C. Identification of cytoskeleton-associated proteins in isolated rat liver endosomes. Biochem. J. 1997, 327:741-746.
75. Sprenger R.R., Speijer D., Back J.W., De Koster C.G., Pannekoek H., Horrevoets A.J. Comparative proteomics of human endothelial cell caveolae and rafts using two-dimensional gel electrophoresis and mass spectrometry. Electrophoresis 2004, 25:156-172.
76. Foster L.J., De Hoog C.L., Mann M. Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:5813-5818.
77. Aboulaich N., Vainonen J.P., Stralfors P., Vener A.V. Vectorial proteomics reveal targeting, phosphorylation and specific fragmentation of polymerase I and transcript release factor (PTRF) at the surface of caveolae in human adipocytes. Biochem. J. 2004, 383:237-248.
78. Hansen C.G., Nichols B.J. Exploring the caves: cavins, caveolins and caveolae. Trends Cell Biol. 2010, 20:177-186.
79. Briand N., Dugail I., Le Lay S. Cavin proteins: new players in the caveolae field. Biochimie 2011, 93:71-77.
80. Hayer A., Stoeber M., Bissig C., Helenius A. Biogenesis of caveolae: stepwise assembly of large caveolin and cavin complexes. Traffic 2010, 11:361-382.
81. Garver W.S., Xie C., Repa J.J., Turley S.D., Dietschy J.M. Niemann-Pick C1 expression is not regulated by the amount of cholesterol flowing through cells in the mouse. J. Lipid Res. 2005, 46:1745-1754.
82. Jackle S., Beisiegel U., Rinninger F., Buck F., Grigoleit A., Block A., Groger I., Greten H., Windler E. Annexin VI, a marker protein of hepatocytic endosomes. J. Biol. Chem. 1994, 269:1026-1032.
83. Ortega D., Pol A., Biermer M., Jackle S., Enrich C. Annexin VI defines an apical endocytic compartment in rat liver hepatocytes. J. Cell Sci. 1998, 111:261-269.
84. Pons M., Ihrke G., Koch S., Biermer M., Pol A., Grewal T., Jackle S., Enrich C. Late endocytic compartments are major sites of annexin VI localization in NRK fibroblasts and polarized WIF-B hepatoma cells. Exp. Cell Res. 2000, 257:33-47.
85. van Duyl B.Y., Meeldijk H., Verkleij A.J., Rijkers D.T., Chupin V., de Kruijff B., Killian J.A. A synergistic effect between cholesterol and tryptophan-flanked transmembrane helices modulates membrane curvature. Biochemistry 2005, 44:4526-4532.
86. Gaus K., Gratton E., Kable E.P., Jones A.S., Gelissen I., Kritharides L., Jessup W. Visualizing lipid structure and raft domains in living cells with two-photon microscopy. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:15554-15559.
87. Owen D.M., Lanigan P.M., Dunsby C., Munro I., Grant D., Neil M.A., French P.M., Magee A.I. Fluorescence lifetime imaging provides enhanced contrast when imaging the phase-sensitive dye di-4-ANEPPDHQ in model membranes and live cells. Biophys. J. 2006, 90:L80-L82.
88. Simons K., Toomre D. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 2000, 1:31-39.
89. Brown D.A., London E. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J. Biol. Chem. 2000, 275:17221-17224.
90. Edidin M. The state of lipid rafts: from model membranes to cells. Annu. Rev. Biophys. Biomol. Struct. 2003, 32:257-283.
91. Hayes M.J., Rescher U., Gerke V., Moss S.E. Annexin-actin interactions. Traffic 2004, 5:571-576.
92. Hayes M.J., Merrifield C.J., Shao D., Ayala-Sanmartin J., Schorey C.D., Levine T.P., Proust J., Curran J., Bailly M., Moss S.E. Annexin 2 binding to phosphatidylinositol 4, 5-bisphosphate on endocytic vesicles is regulated by the stress response pathway. J. Biol. Chem. 2004, 279:14157-14164.
93. Rescher U., Ruhe D., Ludwig C., Zobiack N., Gerke V. Annexin 2 is a phosphatidylinositol (4, 5)-bisphosphate binding protein recruited to actin assembly sites at cellular membranes. J. Cell Sci. 2004, 117:3473-3480.
94. Yin H.L., Janmey P.A. Phosphoinositide regulation of the actin cytoskeleton. Annu. Rev. Physiol. 2003, 65:761-789.
95. Pike L.J., Miller J.M. Cholesterol depletion delocalizes phosphatidylinositol bisphosphate and inhibits hormone-stimulated phosphatidylinositol turnover. J. Biol. Chem. 1998, 273:22298-22304.
96. Kwik J., Boyle S., Fooksman D., Margolis L., Sheetz M.P., Edidin M. Membrane cholesterol, lateral mobility, and the phosphatidylinositol 4, 5-bisphosphate-dependent organization of cell actin. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:13964-13969.
97. Goebeler V., Poeter M., Zeuschner D., Gerke V., Rescher U. Annexin A8 regulates late endosome organization and function. Mol. Biol. Cell 2008, 19:5267-5278.
98. Kobayashi R., Tashima Y. Purification, biological properties and partial sequence analysis of 67-kDa calcimedin and its 34-kDa fragment from chicken gizzard. Eur. J. Biochem. 1990, 188:447-453.
99. Hosoya H., Kobayashi R., Tsukita S., Matsumura F. Ca(2+)-regulated actin and phospholipid binding protein (68 kD-protein) from bovine liver: identification as a homologue for annexin VI and intracellular localization. Cell Motil. Cytoskeleton. 1992, 22:200-210.
100. Goldberg M., Feinberg J., Lecolle S., Kaetzel M.A., Rainteau D., Lessard J.L., Dedman J.R., Weinman S. Co-distribution of annexin VI and actin in secretory ameloblasts and odontoblasts of rat incisor. Cell Tissue Res. 1991, 263:81-89.
101. Monastyrskaya K., Babiychuk E.B., Hostettler A., Wood P., Grewal T., Draeger A. Plasma membrane-associated annexin A6 reduces Ca2+ entry by stabilizing the cortical actin cytoskeleton. J. Biol. Chem. 2009, 284:17227-17242.
102. Patterson R.L., van Rossum D.B., Gill D.L. Store-operated Ca2+ entry: evidence for a secretion-like coupling model. Cell 1999, 98:487-499.
103. Rosado J.A., Sage S.O. The actin cytoskeleton in store-mediated calcium entry. J. Physiol. 2000, 526:221-229.
104. Jardin I., Lopez J.J., Salido G.M., Rosado J.A. Orai1 mediates the interaction between STIM1 and hTRPC1 and regulates the mode of activation of hTRPC1-forming Ca2+ channels. J. Biol. Chem. 2008, 283:25296-25304.
105. Tamarina N.A., Kuznetsov A., Philipson L.H. Reversible translocation of EYFP-tagged STIM1 is coupled to calcium influx in insulin secreting beta-cells. Cell Calcium 2008, 44:533-544.
106. Morales S., Camello P.J., Rosado J.A., Mawe G.M., Pozo M.J. Disruption of the filamentous actin cytoskeleton is necessary for the activation of capacitative calcium entry in naive smooth muscle cells. Cell. Signal. 2005, 17:635-645.
107. Watanabe T., Inui M., Chen B.Y., Iga M., Sobue K. Annexin VI-binding proteins in brain. Interaction of annexin VI with a membrane skeletal protein, calspectin (brain spectrin or fodrin). J. Biol. Chem. 1994, 269:17656-17662.
108. Kamal A., Ying Y., Anderson R.G. Annexin VI-mediated loss of spectrin during coated pit budding is coupled to delivery of LDL to lysosomes. J. Cell Biol. 1998, 142:937-947.
109. Sato K., Saito Y., Kawashima S. Identification and characterization of membrane-bound calpains in clathrin-coated vesicles from bovine brain. Eur. J. Biochem. 1995, 230:25-31.
110. Lin H.C., Sudhof T.C., Anderson R.G. Annexin VI is required for budding of clathrin-coated pits. Cell 1992, 70:283-291.
111. Pons M., Grewal T., Rius E., Schnitgerhans T., Jackle S., Enrich C. Evidence for the involvement of annexin 6 in the trafficking between the endocytic compartment and lysosomes. Exp. Cell Res. 2001, 269:13-22.
112. Beck K.A., Buchanan J.A., Malhotra V., Nelson W.J. Golgi spectrin: identification of an erythroid beta-spectrin homolog associated with the Golgi complex. J. Cell Biol. 1994, 127:707-723.
113. De Matteis M.A., Morrow J.S. The role of ankyrin and spectrin in membrane transport and domain formation. Curr. Opin. Cell Biol. 1998, 10:542-549.
114. Stankewich M.C., Tse W.T., Peters L.L., Ch'ng Y., John K.M., Stabach P.R., Devarajan P., Morrow J.S., Lux S.E. A widely expressed betaIII spectrin associated with Golgi and cytoplasmic vesicles. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:14158-14163.
115. Xu J., Ziemnicka D., Merz G.S., Kotula L. Human spectrin Src homology 3 domain binding protein 1 regulates macropinocytosis in NIH 3T3 cells. J. Cell Sci. 2000, 113:3805-3814.
116. Kusumi A., Shirai Y.M., Koyama-Honda I., Suzuki K.G., Fujiwara T.K. Hierarchical organization of the plasma membrane: investigations by single-molecule tracking vs. fluorescence correlation spectroscopy. FEBS Lett. 2010, 584:1814-1823.
117. D.M. Owen, C. Rentero, J. Rossy, A. Magenau, D. Williamson, M. Rodriguez, K. Gaus, PALM imaging and cluster analysis of protein heterogeneity at the cell surface. J. Biophotonics, 3 (2010) 446-454.
118. Goswami D., Gowrishankar K., Bilgrami S., Ghosh S., Raghupathy R., Chadda R., Vishwakarma R., Rao M., Mayor S. Nanoclusters of GPI-anchored proteins are formed by cortical actin-driven activity. Cell 2008, 135:1085-1097.
119. Rosse C., Linch M., Kermorgant S., Cameron A.J., Boeckeler K., Parker P.J. PKC and the control of localized signal dynamics. Nat. Rev. Mol. Cell Biol. 2010, 11:103-112.
120. Corbalan-Garcia S., Gomez-Fernandez J.C. The C2 domains of classical and novel PKCs as versatile decoders of membrane signals. Biofactors 2010, 36:1-7.
121. Kheifets V., Mochly-Rosen D. Insight into intra- and inter-molecular interactions of PKC: design of specific modulators of kinase function. Pharmacol. Res. 2007, 55:467-476.
122. Steinberg S.F. Structural basis of protein kinase C isoform function. Physiol. Rev. 2008, 88:1341-1378.
123. Mochly-Rosen D. Localization of protein kinases by anchoring proteins: a theme in signal transduction. Science 1995, 268:247-251.
124. Kheifets V., Bright R., Inagaki K., Schechtman D., Mochly-Rosen D. Protein kinase C delta (deltaPKC)-annexin V interaction: a required step in deltaPKC translocation and function. J. Biol. Chem. 2006, 281:23218-23226.
125. Xu T.R., Rumsby M.G. Phorbol ester-induced translocation of PKC epsilon to the nucleus in fibroblasts: identification of nuclear PKC epsilon-associating proteins. FEBS Lett. 2004, 570:20-24.
126. Ron D., Mochly-Rosen D. Agonists and antagonists of protein kinase C function, derived from its binding proteins. J. Biol. Chem. 1994, 269:21395-21398.
127. Schmitz-Peiffer C., Browne C.L., Walker J.H., Biden T.J. Activated protein kinase C alpha associates with annexin VI from skeletal muscle. Biochem. J. 1998, 330:675-681.
128. Freye-Minks C., Kretsinger R.H., Creutz C.E. Structural and dynamic changes in human annexin VI induced by a phosphorylation-mimicking mutation, T356D. Biochemistry 2003, 42:620-630.
129. Fauvel J., Vicendo P., Roques V., Ragab-Thomas J., Granier C., Vilgrain I., Chambaz E., Rochat H., Chap H., Douste-Blazy L. Isolation of two 67 kDa calcium-binding proteins from pig lung differing in affinity for phospholipids and in anti-phospholipase A2 activity. FEBS Lett. 1987, 221:397-402.
130. Davis A.J., Butt J.T., Walker J.H., Moss S.E., Gawler D.J. The Ca2+-dependent lipid binding domain of P120GAP mediates protein-protein interactions with Ca2+-dependent membrane-binding proteins. Evidence for a direct interaction between annexin VI and P120GAP. J. Biol. Chem. 1996, 271:24333-24336.
131. Livneh E., Dull T.J., Berent E., Prywes R., Ullrich A., Schlessinger J. Release of a phorbol ester-induced mitogenic block by mutation at Thr-654 of the epidermal growth factor receptor. Mol. Cell. Biol. 1988, 8:2302-2308.
132. Hunter T., Ling N., Cooper J.A. Protein kinase C phosphorylation of the EGF receptor at a threonine residue close to the cytoplasmic face of the plasma membrane. Nature 1984, 311:480-483.
133. Countaway J.L., McQuilkin P., Girones N., Davis R.J. Multisite phosphorylation of the epidermal growth factor receptor. Use of site-directed mutagenesis to examine the role of serine/threonine phosphorylation. J. Biol. Chem. 1990, 265:3407-3416.
134. Bowen S., Stanley K., Selva E., Davis R.J. Constitutive phosphorylation of the epidermal growth factor receptor blocks mitogenic signal transduction. J. Biol. Chem. 1991, 266:1162-1169.
135. Morrison P., Takishima K., Rosner M.R. Role of threonine residues in regulation of the epidermal growth factor receptor by protein kinase C and mitogen-activated protein kinase. J. Biol. Chem. 1993, 268:15536-15543.
136. Lund K.A., Lazar C.S., Chen W.S., Walsh B.J., Welsh J.B., Herbst J.J., Walton G.M., Rosenfeld M.G., Gill G.N., Wiley H.S. Phosphorylation of the epidermal growth factor receptor at threonine 654 inhibits ligand-induced internalization and down-regulation. J. Biol. Chem. 1990, 265:20517-20523.
137. Bao J., Alroy I., Waterman H., Schejter E.D., Brodie C., Gruenberg J., Yarden Y. Threonine phosphorylation diverts internalized epidermal growth factor receptors from a degradative pathway to the recycling endosome. J. Biol. Chem. 2000, 275:26178-26186.
138. Wang X.Q., Yan Q., Sun P., Liu J.W., Go L., McDaniel S.M., Paller A.S. Suppression of epidermal growth factor receptor signaling by protein kinase C-alpha activation requires CD82, caveolin-1, and ganglioside. Cancer Res. 2007, 67:9986-9995.
139. Sigismund S., Woelk T., Puri C., Maspero E., Tacchetti C., Transidico P., Di Fiore P.P., Polo S. Clathrin-independent endocytosis of ubiquitinated cargos. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:2760-2765.
140. Ringerike T., Blystad F.D., Levy F.O., Madshus I.H., Stang E. Cholesterol is important in control of EGF receptor kinase activity but EGF receptors are not concentrated in caveolae. J. Cell Sci. 2002, 115:1331-1340.
141. Mineo C., Ying Y.S., Chapline C., Jaken S., Anderson R.G. Targeting of protein kinase Calpha to caveolae. J. Cell Biol. 1998, 141:601-610.
142. Prevostel C., Alice V., Joubert D., Parker P.J. Protein kinase C(alpha) actively downregulates through caveolae-dependent traffic to an endosomal compartment. J. Cell Sci. 2000, 113:2575-2584.
143. Downward J., Graves J.D., Warne P.H., Rayter S., Cantrell D.A. Stimulation of p21ras upon T-cell activation. Nature 1990, 346:719-723.
144. Marais R., Light Y., Mason C., Paterson H., Olson M.F., Marshall C.J. Requirement of Ras-GTP-Raf complexes for activation of Raf-1 by protein kinase C. Science 1998, 280:109-112.
145. Matallanas D., Sanz-Moreno V., Arozarena I., Calvo F., Agudo-Ibanez L., Santos E., Berciano M.T., Crespo P. Distinct utilization of effectors and biological outcomes resulting from site-specific Ras activation: Ras functions in lipid rafts and Golgi complex are dispensable for proliferation and transformation. Mol. Cell. Biol. 2006, 26:100-116.
146. Esteban L.M., Vicario-Abejon C., Fernandez-Salguero P., Fernandez-Medarde A., Swaminathan N., Yienger K., Lopez E., Malumbres M., McKay R., Ward J.M., Pellicer A., Santos E. Targeted genomic disruption of H-ras and N-ras, individually or in combination, reveals the dispensability of both loci for mouse growth and development. Mol. Cell. Biol. 2001, 21:1444-1452.
147. Plowman S.J., Hancock J.F. Ras signaling from plasma membrane and endomembrane microdomains. Biochim. Biophys. Acta 2005, 1746:274-283.
148. Hancock J.F. Ras proteins: different signals from different locations. Nat. Rev. Mol. Cell Biol. 2003, 4:373-384.
149. Donovan S., Shannon K.M., Bollag G. GTPase activating proteins: critical regulators of intracellular signaling. Biochim. Biophys. Acta 2002, 1602:23-45.
150. Quilliam L.A., Rebhun J.F., Castro A.F. A growing family of guanine nucleotide exchange factors is responsible for activation of Ras-family GTPases. Prog. Nucleic Acid. Res. Mol. Biol. 2002, 71:391-444.
151. Cullen P.J., Lockyer P.J. Integration of calcium and Ras signalling. Nat. Rev. Mol. Cell Biol. 2002, 3:339-348.
152. Raabe T., Rapp U.R. Ras signaling: PP2A puts Ksr and Raf in the right place. Curr. Biol. 2003, 13:R635-R637.
153. Dhillon A.S., Kolch W. Untying the regulation of the Raf-1 kinase. Arch. Biochem. Biophys. 2002, 404:3-9.
154. Kolch W. Coordinating ERK/MAPK signalling through scaffolds and inhibitors. Nat. Rev. Mol. Cell Biol. 2005, 6:827-837.
155. Sacks D.B. The role of scaffold proteins in MEK/ERK signalling. Biochem. Soc. Trans. 2006, 34:833-836.
156. Grewal T., Tebar F., Pol A., Enrich C. Involvement of targeting and scaffolding proteins in the regulation of the EGFR/Ras/MAPK pathway in oncogenesis. Curr. Signal Transduct. Ther. 2006, 1:147-167.
157. Downward J. Targeting RAS signalling pathways in cancer therapy. Nat. Rev. Cancer 2003, 3:11-22.
158. Yarden Y. The EGFR family and its ligands in human cancer: signalling mechanisms and therapeutic opportunities. Eur. J. Cancer 2001, 37:S3-S8.
159. Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 2000, 103:211-225.
160. Chow A., Gawler D. Mapping the site of interaction between annexin VI and the p120GAP C2 domain. FEBS Lett. 1999, 460:166-172.
161. Cooper J.A., Kashishian A. In vivo binding properties of SH2 domains from GTPase-activating protein and phosphatidylinositol 3-kinase. Mol. Cell. Biol. 1993, 13:1737-1745.
162. Wang Z., Tung P.S., Moran M.F. Association of p120 ras GAP with endocytic components and colocalization with epidermal growth factor (EGF) receptor in response to EGF stimulation. Cell Growth Differ. 1996, 7:123-133.
163. Jones R.B., Gordus A., Krall J.A., MacBeath G. A quantitative protein interaction network for the ErbB receptors using protein microarrays. Nature 2006, 439:168-174.
164. Chow A., Davis A.J., Gawler D.J. Investigating the role played by protein-lipid and protein-protein interactions in the membrane association of the p120GAP CaLB domain. Cell. Signal. 1999, 11:443-451.
165. Chow A., Davis A.J., Gawler D.J. Identification of a novel protein complex containing annexin VI, Fyn, Pyk2 and the p120(GAP)C2. FEBS Lett. 2000, 469:88-92.
166. Blagoev B., Kratchmarova I., Ong S.E., Nielsen M., Foster L.J., Mann M. A proteomics strategy to elucidate functional protein-protein interactions applied to EGF signaling. Nat. Biotechnol. 2003, 21:315-318.
167. Rikova K., Guo A., Zeng Q., Possemato A., Yu J., Haack H., Nardone J., Lee K., Reeves C., Li Y., Hu Y., Tan Z., Stokes M., Sullivan L., Mitchell J., Wetzel R., Macneill J., Ren J.M., Yuan J., Bakalarski C.E., Villen J., Kornhauser J.M., Smith B., Li D., Zhou X., Gygi S.P., Gu T.L., Polakiewicz R.D., Rush J., Comb M.J. Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell 2007, 131:1190-1203.
168. Vishwanatha J.K., Salazar E., Gopalakrishnan V.K. Absence of annexin I expression in B-cell non-Hodgkin's lymphomas and cell lines. BMC Cancer 2004, 4:8.
169. Chetcuti A., Margan S.H., Russell P., Mann S., Millar D.S., Clark S.J., Rogers J., Handelsman D.J., Dong Q. Loss of annexin II heavy and light chains in prostate cancer and its precursors. Cancer Res. 2001, 61:6331-6334.
170. Smythe E., Smith P.D., Jacob S.M., Theobald J., Moss S.E. Endocytosis occurs independently of annexin VI in human A431 cells. J. Cell Biol. 1994, 124:301-306.
171. Boultwood J., Fidler C., Strickson A.J., Watkins F., Gama S., Kearney L., Tosi S., Kasprzyk A., Cheng J.F., Jaju R.J., Wainscoat J.S. Narrowing and genomic annotation of the commonly deleted region of the 5q-syndrome. Blood 2002, 99:4638-4641.
172. Davies A.A., Moss S.E., Crompton M.R., Jones T.A., Spurr N.K., Sheer D., Kozak C., Crumpton M.J. The gene coding for the p68 calcium-binding protein is localised to bands q32-q34 of human chromosome 5, and to mouse chromosome 11. Hum. Genet. 1989, 82:234-238.
173. Moss S.E., Crumpton M.J. Alternative splicing gives rise to two forms of the p68 Ca2(+)-binding protein. FEBS Lett. 1990, 261:299-302.
174. Edwards H.C., Moss S.E. Functional and genetic analysis of annexin VI. Mol. Cell. Biochem. 1995, 149-150:293-299.
175. Fleet A., Ashworth R., Kubista H., Edwards H., Bolsover S., Mobbs P., Moss S.E. Inhibition of EGF-dependent calcium influx by annexin VI is splice form-specific. Biochem. Biophys. Res. Commun. 1999, 260:540-546.
176. Strzelecka-Kiliszek A., Buszewska M.E., Podszywalow-Bartnicka P., Pikula S., Otulak K., Buchet R., Bandorowicz-Pikula J. Calcium- and pH-dependent localization of annexin A6 isoforms in Balb/3T3 fibroblasts reflecting their potential participation in vesicular transport. J. Cell. Biochem. 2008, 104:418-434.
177. Huber R., Schneider M., Mayr I., Romisch J., Paques E.P. The calcium binding sites in human annexin V by crystal structure analysis at 2.0 A resolution. Implications for membrane binding and calcium channel activity. FEBS Lett. 1990, 275:15-21.
178. Kawasaki H., Avila-Sakar A., Creutz C.E., Kretsinger R.H. The crystal structure of annexin VI indicates relative rotation of the two lobes upon membrane binding. Biochim. Biophys. Acta 1996, 1313:277-282.
179. Turro S., Ingelmo-Torres M., Estanyol J.M., Tebar F., Fernandez M.A., Albor C.V., Gaus K., Grewal T., Enrich C., Pol A. Identification and characterization of associated with lipid droplet protein 1: a novel membrane-associated protein that resides on hepatic lipid droplets. Traffic 2006, 7:1254-1269.
180. Kastl K., Ross M., Gerke V., Steinem C. Kinetics and thermodynamics of annexin A1 binding to solid-supported membranes: a QCM study. Biochemistry 2002, 41:10087-10094.
181. Babiychuk E.B., Monastyrskaya K., Draeger A. Fluorescent annexin A1 reveals dynamics of ceramide platforms in living cells. Traffic 2008, 9:1757-1775.
182. Harder T., Kellner R., Parton R.G., Gruenberg J. Specific release of membrane-bound annexin II and cortical cytoskeletal elements by sequestration of membrane cholesterol. Mol. Biol. Cell 1997, 8:533-545.
183. Morel E., Parton R.G., Gruenberg J. Annexin A2-dependent polymerization of actin mediates endosome biogenesis. Dev. Cell 2009, 16:445-457.
184. Calpe-Berdiel L., Escola-Gil J.C., Julve J., Zapico-Muniz E., Canals F., Blanco-Vaca F. Differential intestinal mucosal protein expression in hypercholesterolemic mice fed a phytosterol-enriched diet. Proteomics 2007, 7:2659-2666.
185. Dillon S.R., Mancini M., Rosen A., Schlissel M.S. Annexin V binds to viable B cells and colocalizes with a marker of lipid rafts upon B cell receptor activation. J. Immunol. 2000, 164:1322-1332.