Annexins and ATP in membrane traffic: a comparison with membrane fusion machinery

• Autorzy: Bandorowicz-Pikula J. , Pikula S.
• Języki publikacji: EN

Abstrakty

EN

Annexins, calcium- and membrane-binding multifunctional proteins, have been implicated in N-ethylmaleimide (NEM)-independent fusion of vesicular structures involved in membrane traffic. This view is based on intracellular localization of annexins, which frequently associated with endosomes, chromaffin granules, caveolae, clathrin-coated pits, and other membrane compartments, engaged in endo- and exocytosis. Moreover, annexins were found to modulate budding and aggregation of vesicle membranes, to interact with cytoskeletal proteins, and, upon binding to membranes, to change the structure of lipid bilayer, leading to membrane fusion. In addition, some annexins are substrates for various protein kinases and, in membrane-bound form, reveal calcium channel activity. Recently, annexins were observed to interact in vitro and in vivo with nucleotides, ATP, GTP or cAMP, which are potent mediators of membrane traffic processes. In addition, annexin VII showed hydrolytic activity towards GTP, and similarities in the mechanism of action to that of small GTP-binding proteins were found. The aim of the present review is to summarize the observations implying annexins as possible effectors in endo- and exocytosis and to compare them with well known complexes of cytosolic and membrane proteins forming the true membrane fusion machinery within a cell, conserved from yeast to the neurons of humans.

Słowa kluczowe

EN

membrane traffic process; calcium channel; vesicle membrane; lipid bilayer; cytoskeletal protein; membrane; membrane fusion; intracellular localization; N-ethylmaleimide; nucleotide; protein kinase; annexin

• Wydawca: -
• Czasopismo: Acta Biochimica Polonica
• Rocznik: 1998
• Tom: 45
• Numer: 3
• Opis fizyczny: p.721-733,fig.

Twórcy

autor

Bandorowicz-Pikula J.

• M.Nencki Institute of Experimental Biology, L.Pasteur 3, 02-093 Warsaw, Poland

autor

Pikula S.

Bibliografia

• 1. Woodman, P.G. (1997) The roles of NSF, SNAPs and SNAREs during membrane fu­sion. Biochim. Riophys. Acta 1357, 155-172.
• 2. Bock, J.B. & Scheller, R.H. (1997) A fusion of new ideas. Nature 387, 133-135.
• 3. Hay, J.C. & Scheller, R.H. (1997) SNAREs and NSF in targeted membrane fusion. Curr. Opin. Cell Biol. 9, 505-512.
• 4. Martin, T.F.J. (1997) Stages of regulated exo- cytosis. Trends Cell Biol. 7, 271-276.
• 5. Garner, C.C. & Kindler, S. (1996) Synaptic proteins ana the assembly of synaptic junc­tions. Trends Cell Biol. 6, 429-433.
• 6. Morimoto, T. & Ogihara. S. (1996) ATP is re­quired in platelet serotonin exocytosis for pro­tein phosphorylation and priming of secretory vesicles docked on the plasma membrane. J. Cell ScL 109, 113-118.
• 7. Regazzi, R., Sadoul, K., Meda, P., Kelly, R.B., Halban, P.A. & Wollheim, C.B. (1996) Muta­tional analysis of VAMP domains implicated in Ca -induced insulin exocytosis. EMBO J. 15, 6951-6959.
• 8. Cohen, B.E., Lee, G., Arispe, N. & Pollard, H.B. (1995) Cyclic 3'-5' adenosine monophos­phate binds to annexin I and regulates cal­cium-dependent membrane aggregation and ion channel activity. FEBS Lett. 377, 444- 450.
• 9. Caohuy, H.. Srivastava, M. & Pollard, H.B. (1996) Membrane fusion protein synexin (an- nexin VII) as a Ca /GTP sensor in exocytotic secretion. Proc. Natl. Acad. Sci. U.S.A. 93, 10797-10802.
• 10. Bandorowicz-Pikula, J. & Awasthi, Y.C. (1997) Interaction of annexins IV and VI with ATP. An alternative mechanism by which a cellular function of these calcium- and membrane- binding proteins is regulated. FEBS Lett. 409, 300-306.
• 11. Bandorowicz Pikula, J., Wrzosek, A., Pikula, S. & Awasthi, Y.C. (1997) Fluorescence spec­troscopic studies on interactions between liver annexin VI and nucleotides: A possible role for a tryptophan residue. Eur. J. Biochem. 248, 238-244.
• 12. Pollard, H.B, Caohuy, H., Minton, A.P. & Sri­vastava, M. (1998) Synexin (annexin VII) hy- 729 pothesis for Ca" /GTP-regulated exocytosis. Adv. Pharmacol 42, 81-87.
• 13. Siidhof, T.C. (1995) The synaptic vesicle cycle: A cascade of protein-protein interaction. Na­ture 375, 645-653.
• 14. Sollner, T.H. (1995) SNAREs and targeted membrane fusion. FEBS Lett. 369, 80-83.
• 15. Terrian, D.M. & White, M.K. (1997) Phyloge- netic analysis of membrane trafficking pro­teins: A family reunion and secondary struc­ture predictions. Eur. J. Cell Biol. 73, 198- 204.
• 16. DiDonato, M. & Sarkar, B. (1997) Copper transport and its alterations in Menkes and Wilson diseases. Biochim. Biophys. Acta 1360, 3-16.
• 17. Petris, M.J., Mercer, J.F., Culvenor, J.G., Lockhart, P., Gleeson, P.A. & Camakaris, J. (1996) Ligand-regulated transport of the Men­kes copper P-type ATPase efflux pump from the Golgi apparatus to the plasma membrane: A novel mechanism of regulated trafficking. EMBO J. 15,6084-6095.
• 18. Pikula, S., Bandorowicz-Pikula, J., Awasthi, S. & Awasthi, Y.C. (1996) ATP-driven efflux of glutathione S-conjugates, antitumor drugs, and xenobiotics from human erythrocytes. Biochem. Arch. 12, 261-271.
• 19. Makowski, P. & Pikula, S. (1997) Participation of the multispecific organic anion transporter in hepatobiliary cxcretion of glutathione S- conjugates, drugs and other xenobiotics. Pol. J. Pharmacol. 49, 387-394.
• 20. Awasthi, Y.C., Awasthi, S. & Zimniak, P. (1997) Multiple transport proteins involved in the detoxification of endo- and xenobiotics. Frontiers BioscL 2, d427-d437.
• 21. Roelofsen, H., Vos, T.A., Schippers, I.J., Kui- pers, F., Koning, H., Moshage, H., Jansen, P.L. & Muller, M. (1997) Increased levels of the multidrug resistance protein in lateral membranes of proliferating hepatocyte- derived cells. Gastroenterology 112,511-521.
• 22. Sollner, T.li & Rothman, J.E. (1996) Molecu­lar machinery mediating vesicle budding, docking and fuoion. Experientia 52, 1021- 1025.
• 23. Hosaka, M. & Siidhof, T.C. (1998) Synapsins I and II are ATP-binding proteins with differen­tial Ca2* regilation. J. Biol. Chem, 273,1425- 1429.
• 24. Esser, L., Wang, C.-R., Hosaka, M., Smagula, C.S., Siidhof, T.C. & Deisenhofcr, J. (1998) Synapsin I is structurally similar to ATP- utilizing enzymes. EMBO J. 17, 977-984.
• 25. Bennett, MX (1995) SNAREs and specificity of transport vesicle targeting. Curr. Opin. Cell Biol. 7, 581-586.
• 26. Whiteheart, S.W. & Kubalek, E.W. (1995) SNAPs and NSF: General members of the fu­sion apparatus. Trends Cell Biol 5, 64-68.
• 27. Orci, L., Stamnes, M., Ravazzola, M., Am- herdt, M., Perrelet, A., Sollner, T.H. & Roth­man, J.E. (1997) Bidirectional transport by distinct populations of COPI-coated vesicles. Cell 90, 335-349.
• 28. Gutierrez, L.M.. Viniegra, S., Rueda, J., Ferrer-Montiel, A.V., Canaves, J.M. & Montal, M. (1997) A peptide that mimics the C- terminal sequence of SNAP-25 inhibits secre­tory vesicle docking in chromaffin cells. J. Biol. Chem. 272, 2634-2639.
• 29. Bean, A.J., Seifert, R., Chen, Y.A., Sacks, R. & Scheller, R.H. (1997) Hrs-2 is an ATPase impli­cated in calcium-regulated secretion. Nature 385, 826-829.
• 30. De Waard, M., Liu, H., Walker, D., Scott, V.E.S., Gurnett, Ch.A. & Campbell, K.P. (1997) Direct binding of G-protein/fy complex to voltage-dependent calcium channels. Nature 385, 446-450.
• 31. Gruenberg, J. & Maxfield, F.R. (1995) Mem- brane transport in the endocytic pathway. Curr. Opin. Cell Biol. 7, 552-563.
• 32. Monck, J.R. & Fernandez, J.M. (1996) The fu­sion pore and mechanisms of biological mem­brane fusion. Curr. Opin. Cell Biol. 8, 524- 533.
• 33. Hughson, F.M. (1995) Molecular mechanism of protein-mediated membrane fusion. Curr. Opin. Struct. Biol. 5, 507-513.
• 34. Edelmann, L., Hanson, P.I., Chapman, E.R. & Jahn, R. (1995) Synaptobrevin binding to syn- aptophysin: A potential mechanism for con­trolling the exocytotic fusion machine. EMBO J. 14, 224-231.
• 35. Monck, J.R., Oberhauser, A.F. & Fernandez, J.M. (1995) The exocytotic fusion pore inter­face: A model of the site of neurotransmitter release. Mol. Membr. Biol 12, 151-156.
• 36. Bandorowicz, J. & Pikula, S. (1993) Annexins — multifunctional, calcium-dependent, phos- pholipid-binding proteins. Acta Biochim. Polon. 40, 281-293.
• 37. Gerke, V. & Moss, S.E. (1997) Annexins and membrane dynamics. Biochim. Biophys. Acta 1357, 129-154.
• 38. Gruenberg, J. & Emans, N. (1993) Annexins in membrane traffic. Trends Cell Biol 3, 224- 227.
• 39. Burgoyne, R.D. & Clague, M.J. (1994) Annexin in the endocytic pathway. Trends Biochem. S!ci. 19,231-232.
• 40. Mayorga, L.S., Beron, W., Sorrouf, M.N., Co­lombo, M.I., Creutz, C. & Stahl, P.D. (1994) Calcium-dependent fusion among endosomes. J. Biol Chem. 269, 30927-30934.
• 41. Nakata, T., Sobue, K. & Ilirokawa, N. (1990) Conformational change and localization of cal- pactin I complex involved in exocytosis as re­vealed by quick-freeze, deep-etch electron mi­croscopy and immunocytochemistry. J. Cell Biol 110, 13-25.
• 42. Emans, N., Govel, J.-P., Walter, C., Gerke, V., Kellner, R., Griffiths, G. & Gruenberg, J. (1993) Annexin II a major component of fuso-genie endosomal vesicles. J. Cell Biol 120, 1357-1369.
• 43.Senda, T., Okabe, T.. Matsuda, M. & Fujita, H. (1994) Quick-freeze, deep-etch visualization of exocytosis in anterior pituitary secretory cells: Localization and possible roles of actin and an- nexin II. Cell Tissue Res. 277, 51-60.
• 44. Jost, M., Zeuschner, D., Seemann, J. & Gerke, K. (1997) Identification and characterization of a novel type of annexin-membrane interacotion: Ca is not required for the association of annexin II with early endosomes. J. Cell Sci. 110,221-228.
• 45. Diakonova, M., Gerke, V., Ernst, J., Liautard, J.P., van der Vusse, G. & Griffiths, G. (1997) Localization of five annexins in J774 macro­phages and on isolated phagosomes. J. Cell SciI 110, 1199-1213.
• 46.Sagot, I., Regnouf, F., Henry, J.-P. & Pradel, L.-A. (1997) Translocation of cytosolic an­nexin 2 to a Triton-insoluble membrane subdo- main upon nicotine stimulation of chromaffin cultured cells. FEBS Lett 410, 229-234.
• 47. Jackie, S., Beisiegel, U., Rinninger, F., Buck, F., Grigoleit, A., Block, A., Groger, I., Greten, H. & Windier, E. (1994) Annexin VI, a marker protein of hepatocytic endosomes. J. Biol Chem. 269, 1026-1032.
• 48. Schnitzer, J.E., Liu, J. & Oh, P. (1995) Endo­thelial caveolae have the molecular transport machinery for vesicle budding, docking, and fusion including VAMP, NSF, SNAP, annex­ins, and GTPases. J. Biol Chem. 24, 14399- 14404.
• 49. Moss, S.E. (1997) Annexins. Trends Cell Biol 7, 87-89.
• 50. Rainteau, D., Mansuelle, P., Rochat, H. & We­inman, S. (1995) Characterization and ultra- structural localization of annexin VI from mi­tochondria. FEBS Lett. 360, 80-84.
• 51. Pol, A., Ortega, D. & Enrich, C. (1997) Identifi­cation of cycoskeleton-associated proteins in isolated rat liver endosomes. Biochem. J. 327, 741-746.
• 52.Ortega, D., Pol, A., Biermer, M. & Enrich, S. (1998) Annexin VI defines an apical endocytic compartment in rat liver hepatocytes. J. Cell Sci. Ill, 261-269.
• 53. Lin, H., Sudhof, T.C. & Anderson, R.G.W. (1992) Annexin VI is required for budding of clathrin-coated pits. Cell 70, 283-291.
• 54. Evans, T.C. & Nelsestuen, G.L. (1994) Calcium and membrane-binding properties of mono­melic and multimeric annexin II. Biochemistry 33,13231-13238.
• 55. De la Fuente, M. & Parra, A.V. (1995) Vesicle aggregation by annexin I: Role of a secondary membrane binding site. Biochemistry 34, 10393-10399.
• 56. Nelson, M.R. & Creutz, C.E. (1995) Combina­torial mutagenesis of the four domains of an­nexin IV: Effects on chromaffin granule bind­ing and aggregating activities. Biochemistry 34, 3121-3132.
• 57. Raynal, P.R. & 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.
• 58. Giambanco, I., Verzini, M. & Donato, R. (1993) Annexins V and VI in rat tissues during post­natal development: Immunochemical meas­urements. Biochem. Biophys. Res. Commun. 196, 1221-1226.
• 59. Hosoya, II., Kobayashi, R., Tsukita, S. & Matosumura, F. (1992) Ca -regulated actin and phospholipid binding protein (68-kDa protein) from bovine liver: Identification as a homo- logue for annexin VI and intracellular localiza­tion. Cell Motil CytoskeL 22, 200-210.
• 60. Tagoe, C.E., Boustead, C.M., Higgins, S.J. & Walker, J.H. (1994) Characterization and im- munolocalization of rat liver annexin VI. Bio­chim. Biophys. Acta 1192, 272-280.
• 61. Trotter, J.P., Orchard, M.A. & Walker, J.H. (1997) Relocation of annexin V to platelet membranes is a phosphorylation-dcpcndent process. Biochem. J. 328, 447-452.
• 62. Bandorowicz-Pikula, J. & Pikula. S. (1998) Modulation of annexin Vl-driven aggregation of phosphaticiylserine liposomes by ATP. Bio- chimie, in press.
• 63. Bandorowic7.-Pikula, J., Wrzosek, A., Ma- kowski, P. & Pikula, S. (1997) The relationship between the binding of ATP and calcium to an­nexin IV. Effect of nucleotide on the calcium- dependent interaction of annexin with phos- phatidylserine. Mol Membr. Biol. 14, 179- 186.
• 64. Szewczyk, A. & Pikula, S. (1998) Adenosine 5'- triphosphate: An intracellular metabolic mes­senger. Biochim. Biophys. Acta 1365, 333- 353.
• G5.Yoshida, M. & Amano, T. (1995) A common to­pology of proteins catalyzing ATP-triggered re­actions. FEBS Lett. 359, 1-5.
• 66. Bandorowicz Pikula, J. (1998) A nucleotide- binding domain of porcinc liver annexin VI. Proteolysis of annexin VI labeled with 8-azido- ATP, purification of proteolytic fragments by affinity chromatography on ATP-agarose and fluorescence studies. Mol Cell Biochem. 181, 11-20.
• 67. Bombardier, H., Wong, P. & Gicquaud, C. (1997) Effects of nucleotides on the denatura- tion of F-actin: A differential scanning color- imetry and FTIR spectroscopy study. Biochem. Biophys. Res. Commun. 236, 798-803.
• 68. ltaimbault, C., Besson, F. & Buchet, R. (1997) Conformational changes of arginine kinase in­duced by photochemical release of nucleotides from caged nucleotides — an infrared dif- ference-spectroscopy investigation. Eur. J. Biochem. 244, 343-351.
• 69. Matsuda, R., Kaneko, N. & Horikawa, Y. (1997) Presence and comparison of Ca2~ transport activity of annexins I, II, V and VI in large unilamellar vesicles. Biochem. Biophys. Res. Commun. 237, 499-503.
• 70. Benz, J., Bergner, A., Hofmann, A., Demange, P., Göttig, P., Liemann, S., Huber, R. & Voges, D. (1996) The structure of recombinant hu­man annexin VI in crystals and membrane- bound. J. Mol Biol 260, 638-643.
• 71. Luecke, H., Chang. B.T., Mailliard, W.S., Schlaepfer, D.D. & Haigier, H.T. (1995) Crys­tal structure of the annexin XII hexamer and implications for bilayer insertion. Nature 378, 512-515.
• 72. Burger, A.. Berendes, R., Liemann, S., Benz, J., Hofmann, A., Göttig, P., Huber, R., Gerke, V., Thiel, C., Römisch, J. & Weber, K. (1996) The crystal structure and ion channel activity of human annexin II, a peripheral membrane protein. J. Mol Biol 257, 839-847.
• 73. Kaneko, N., Ago, H., Matsuda, R., Inagaki, E. & Miyano, M. (1997) Crystal structure of an­nexin V with its ligand K-201 as a calcium ac­tivity inhibitor. J. Mol Biol 274, 16-20.
• 74. Brisson, A., Mosser, G. & Huber, R. (1991) Structure of soluble and membrane-bound hu­man annexin V. J. Mol Biol 220. 199-203.
• 75.Swairjo, M.A. & Seaton, B.A. (1994) Annexin structure and membrane interactions: A mo­lecular perspective. Annu. Rev. Biophys. Bio- mol Struct. 23, 193-213.
• 76. Liemann, S. & Huber. R. (1997) Three-di- mensional structure of annexins. Cell Mol Life Sei. 53, 516-521.
• 77. Roth, D., Morgan, A. & Burgoyne, R.D. (1993) Identification of a key domain in annexin and 14-3-3 proteins that stimulate calcium-de­pendent exocytosis in permeabilized adrenal chromaffin cells. FEBS Lett 320, 207-210.
• 78. Nelson, T.J., Cavallaro, S., Yi, C.-L., McPhie, D., Schreurs, B.G., Guscv, P.A., Favit, A., Zo- har, 0., Kim, J., Beushausen, S., Ascoli. G., Olds, J., Neve, R. & Alkon, D.L. (1996) Calex- citin: A signaling protein that binds calcium and GTP, inhibits potassium channels, and en­hances membrane excitability. Proc. Natl. Acad. Sci. U.S.A. 93, 13808-13813.
• 79.Nuoffer, C. & Balch, W.E. (1994) GTPases: Multifunctional molecular switches regulating vesicular traffic. Anniu Rev. Biochem. 63, 949-990.
• 80. Olkkonen, V.M. & Stenmark, H. (1997) Role of Rab GTPases in membrane traffic. InL Rev. CytoL 176, 13-85.
• 81. Novick, P. & Zerial, M. (1997) The diversity of Rab proteins in vesicle transport. Curr. Opin. Cell Biol. 9, 496-504.