Phosphatidylinositol 4,5-bisphosphate (PtdIns(4,5)P2) specifically induces membrane penetration and deformation by Bin/Amphiphysin/Rvs (BAR) domains

Journal of Biological Chemistry

Volumn 287, Issue 41, 2012, Pages 34078-34090

  Yoon, Youngdae ^a   Zhang, Xiuqi ^a   Cho, Wonhwa ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHIPHILICS; CELLULAR PROTEINS; DIFFERENT MECHANISMS; DOMAIN-CONTAINING PROTEINS; ENDOPHILIN; FLUORESCENCE IMAGING; HEK293 CELLS; MEMBRANE PENETRATION; MEMBRANE-BOUND; N-TERMINALS; PHOSPHATIDYLINOSITOL 4 ,5-BISPHOSPHATE; SELF-ASSOCIATIONS; UNIVERSAL MECHANISMS;

ASSOCIATION REACTIONS; CELL MEMBRANES; DEFORMATION; MOLECULAR BIOLOGY; PROTEINS;

MEMBRANES;

AMPHIPHYSIN; BIN AMPHIPHYSIN RVS DOMAIN PROTEIN; CELL PROTEIN; CLATHRIN; ENDOPHILIN; ENDOPHILIN A1; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; CELL LEVEL; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; DEPLETION; DROSOPHILA; ENDOCYTOSIS; FLUORESCENCE IMAGING; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; RAT;

ACYLTRANSFERASES; ANIMALS; CELL MEMBRANE; CLATHRIN; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENDOCYTOSIS; FORKHEAD TRANSCRIPTION FACTORS; HEK293 CELLS; HUMANS; NERVE TISSUE PROTEINS; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RATS;

EID: 84867274657     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.372789     Document Type: Article

References (71)

1. McMahon, H. T., and Gallop, J. L. (2005) Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438, 590-596 (Pubitemid 41740562)
2. McNiven, M. A., and Thompson, H. M. (2006) Vesicle formation at the plasma membrane and trans-Golgi network: the same but different. Science 313, 1591-1594 (Pubitemid 44414025)
3. Chernomordik, L. V., and Kozlov, M. M. (2003) Protein-lipid interplay in fusion and fission of biological membranes. Annu. Rev. Biochem. 72, 175-207 (Pubitemid 36930445)
4. Farsad, K., and De Camilli, P. (2003) Mechanisms of membrane deformation. Curr. Opin. Cell Biol. 15, 372-381 (Pubitemid 36928038)
5. Zimmerberg, J., and Kozlov, M. M. (2006) How proteins produce cellular membrane curvature. Nat. Rev. Mol. Cell Biol. 7, 9-19 (Pubitemid 43361568)
6. McMahon, H. T., and Boucrot, E. (2011) Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 12, 517-533
7. Antonny, B. (2011) Mechanisms of membrane curvature sensing. Annu. Rev. Biochem. 80, 101-123
8. Cho, W., and Stahelin, R. V. (2005) Membrane-protein interactions in cell signaling and membrane trafficking. Annu. Rev. Biophys. Biomol. Struct. 34, 119-151 (Pubitemid 40847721)
9. Itoh, T., and De Camilli, P. (2006) BAR, F-BAR (EFC) and ENTH/ANTH domains in the regulation of membrane-cytosol interfaces and membrane curvature. Biochim. Biophys. Acta 1761, 897-912 (Pubitemid 44332330)
10. Habermann, B. (2004) The BAR-domain family of proteins: a case of bending and binding? EMBO Rep. 5, 250-255
11. Dawson, J. C., Legg, J. A., and Machesky, L. M. (2006) Bar domain proteins: a role in tubulation, scission and actin assembly in clathrin-mediated endocytosis. Trends Cell Biol. 16, 493-498 (Pubitemid 44442959)
12. Heath, R. J., and Insall, R. H. (2008) F-BAR domains: multifunctional regulators of membrane curvature. J. Cell Sci. 121, 1951-1954 (Pubitemid 352015191)
13. Frost, A., Unger, V. M., and De Camilli, P. (2009) The BAR domain superfamily: membrane-molding macromolecules. Cell 137, 191-196
14. Ford, M. G., Mills, I. G., Peter, B. J., Vallis, Y., Praefcke, G. J., Evans, P. R., and McMahon, H. T. (2002) Curvature of clathrin-coated pits driven by epsin. Nature 419, 361-366
15. Peter, B. J., Kent, H. M., Mills, I. G., Vallis, Y., Butler, P. J., Evans, P. R., and McMahon, H. T. (2004) BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303, 495-499 (Pubitemid 38120842)
16. Tsujita, K., Suetsugu, S., Sasaki, N., Furutani, M., Oikawa, T., and Takenawa, T. (2006) Coordination between the actin cytoskeleton and membrane deformation by a novel membrane tubulation domain of PCH proteins is involved in endocytosis. J. Cell Biol. 172, 269-279 (Pubitemid 43112973)
17. 2-rich membranes by an inverse BAR domain-like mechanism. J. Cell Biol. 176, 953-964
18. Zhang, B., and Zelhof, A. C. (2002) Amphiphysins: raising the BAR for synaptic vesicle recycling and membrane dynamics. Bin-Amphiphysin- Rvsp. Traffic 3, 452-460 (Pubitemid 34692975)
19. Takei, K., Slepnev, V. I., Haucke, V., and De Camilli, P. (1999) Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat. Cell Biol. 1, 33-39 (Pubitemid 129495007)
20. Farsad, K., Ringstad, N., Takei, K., Floyd, S. R., Rose, K., and De Camilli, P. (2001) Generation of high curvature membranes mediated by direct endophilin bilayer interactions. J. Cell Biol. 155, 193-200 (Pubitemid 34289294)
21. Zimmerberg, J., and McLaughlin, S. (2004) Membrane curvature: how BAR domains bend bilayers. Curr. Biol. 14, R250-252 (Pubitemid 38431278)
22. Weissenhorn, W. (2005) Crystal structure of the endophilin-A1 BAR domain. J. Mol. Biol. 351, 653-661
23. Masuda, M., Takeda, S., Sone, M., Ohki, T., Mori, H., Kamioka, Y., and Mochizuki, N. (2006) Endophilin BAR domain drives membrane curvature by two newly identified structure-based mechanisms. EMBO J. 25, 2889-2897 (Pubitemid 43980395)
24. Gallop, J. L., Jao, C. C., Kent, H. M., Butler, P. J., Evans, P. R., Langen, R., and McMahon, H. T. (2006) Mechanism of endophilin N-BAR domain-mediated membrane curvature. EMBO J. 25, 2898-2910 (Pubitemid 43980396)
25. Aspenstrom, P., Fransson, A., and Richnau, N. (2006) Pombe Cdc15 homology proteins: regulators of membrane dynamics and the actin cytoskeleton. Trends Biochem. Sci. 31, 670-679 (Pubitemid 44791944)
26. Chitu, V., and Stanley, E. R. (2007) Pombe Cdc15 homology (PCH) proteins: coordinators of membrane-cytoskeletal interactions. Trends Cell Biol. 17, 145-156 (Pubitemid 46341827)
27. Itoh, T., Erdmann, K. S., Roux, A., Habermann, B., Werner, H., and De Camilli, P. (2005) Dynamin and the actin cytoskeleton cooperatively regulate plasma membrane invagination by BAR and F-BAR proteins. Dev. Cell 9, 791-804 (Pubitemid 41724107)
28. Kamioka, Y., Fukuhara, S., Sawa, H., Nagashima, K., Masuda, M., Matsuda, M., and Mochizuki, N. (2004) A novel dynamin-associating molecule, formin-binding protein 17, induces tubular membrane invaginations and participates in endocytosis. J. Biol. Chem. 279, 40091-40099 (Pubitemid 39258284)
29. Shimada, A., Niwa, H., Tsujita, K., Suetsugu, S., Nitta, K., Hanawa-Suetsugu, K., Akasaka, R., Nishino, Y., Toyama, M., Chen, L., Liu, Z. J., Wang, B. C., Yamamoto, M., Terada, T., Miyazawa, A., Tanaka, A., Sugano, S., Shirouzu, M., Nagayama, K., Takenawa, T., and Yokoyama, S. (2007) Curved EFC/F-BAR-domain dimers are joined end to end into a filament for membrane invagination in endocytosis. Cell 129, 761-772 (Pubitemid 46813111)
30. Frost, A., Perera, R., Roux, A., Spasov, K., Destaing, O., Egelman, E. H., De Camilli, P., and Unger, V. M. (2008) Structural basis of membrane invagination by F-BAR domains. Cell 132, 807-817 (Pubitemid 351320580)
31. Millard, T. H., Bompard, G., Heung, M. Y., Dafforn, T. R., Scott, D. J., Machesky, L. M., and Fütterer, K. (2005) Structural basis of filopodia formation induced by the IRSp53/MIM homology domain of human IRSp53. EMBO J. 24, 240-250 (Pubitemid 40216129)
32. Lee, S. H., Kerff, F., Chereau, D., Ferron, F., Klug, A., and Dominguez, R. (2007) Structural basis for the actin-binding function of missing-in-metastasis. Structure 15, 145-155 (Pubitemid 46209813)
33. Pykäläinen, A., Boczkowska, M., Zhao, H., Saarikangas, J., Rebowski, G., Jansen, M., Hakanen, J., Koskela, E. V., Peränen, J., Vihinen, H., Jokitalo, E., Salminen, M., Ikonen, E., Dominguez, R., and Lappalainen, P. (2011) Pink-bar is an epithelial-specific BAR domain protein that generates planar membrane structures. Nat. Struct. Mol. Biol. 18, 902-907
34. Bagatolli, L. A., and Gratton, E. (1999) Two-photon fluorescence microscopy observation of shape changes at the phase transition in phospholipid giant unilamellar vesicles. Biophys. J. 77, 2090-2101 (Pubitemid 29463170)
35. 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 (Pubitemid 43049245)
36. Yoon, Y., Tong, J., Lee, P. J., Albanese, A., Bhardwaj, N., Källberg, M., Digman, M. A., Lu, H., Gratton, E., Shin, Y. K., and Cho, W. (2010) Molecular basis of the potent membrane-remodeling activity of the epsin 1 N-terminal homology domain. J. Biol. Chem. 285, 531-540
37. Stahelin, R. V., Digman, M. A., Medkova, M., Ananthanarayanan, B., Rafter, J. D., Melowic, H. R., and Cho, W. (2004) Mechanism of diacylglycerol-induced membrane targeting and activation of protein kinase Cδ. J. Biol. Chem. 279, 29501-29512 (Pubitemid 38915830)
38. Digman, M. A., Dalal, R., Horwitz, A. F., and Gratton, E. (2008) Mapping the number of molecules and brightness in the laser scanning microscope. Biophys. J. 94, 2320-2332
39. Stahelin, R. V., and Cho, W. (2001) Differential roles of ionic, aliphatic, and aromatic residues in membrane-protein interactions: a surface plasmon resonance study on phospholipases A2. Biochemistry 40, 4672-4678 (Pubitemid 32374655)
40. Stahelin, R. V., and Cho, W. (2001) Roles of calcium ions in the membrane binding of C2 domains. Biochem. J. 359, 679-685 (Pubitemid 33063393)
41. Ananthanarayanan, B., Stahelin, R. V., Digman, M. A., and Cho, W. (2003) Activation mechanisms of conventional protein kinase C isoforms are determined by the ligand affinity and conformational flexibility of their C1 domains. J. Biol. Chem. 278, 46886-46894 (Pubitemid 37452270)
42. Cho, W., Bittova, L., and Stahelin, R. V. (2001) Membrane binding assays for peripheral proteins. Anal. Biochem. 296, 153-161 (Pubitemid 32868495)
43. Medkova, M., and Cho, W. (1998) Differential membrane-binding and activation mechanisms of protein kinase C-α and -∈. Biochemistry 37, 4892-4900 (Pubitemid 28175971)
44. 2 is necessary for its interfacial catalysis and arachidonate specificity. Biochemistry 37, 14128-14136
45. Blatner, N. R., Stahelin, R. V., Diraviyam, K., Hawkins, P. T., Hong, W., Murray, D., and Cho, W. (2004) The molecular basis of the differential subcellular localization of FYVE domains. J. Biol. Chem. 279, 53818-53827 (Pubitemid 40051891)
46. Lee, B. I., Yoon, E. T., and Cho, W. (1996) Roles of surface hydrophobic residues in the interfacial catalysis of bovine pancreatic phospholipase A2. Biochemistry 35, 4231-4240
47. Di Paolo, G., and De Camilli, P. (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443, 651-657 (Pubitemid 44564702)
48. McLaughlin, S., and Murray, D. (2005) Plasma membrane phosphoinositide organization by protein electrostatics. Nature 438, 605-611 (Pubitemid 41740564)
49. 2 and proteins: interactions, organization, and information flow. Annu. Rev. Biophys. Biomol. Struct. 31, 151-175
50. Stahelin, R. V., Long, F., Diraviyam, K., Bruzik, K. S., Murray, D., and Cho, W. (2002) Phosphatidylinositol 3-phosphate induces the membrane penetration of the FYVE domains of Vps27p and Hrs. J. Biol. Chem. 277, 26379-26388 (Pubitemid 34967131)
51. Stahelin, R. V., Burian, A., Bruzik, K. S., Murray, D., and Cho, W. (2003) Membrane binding mechanisms of the PX domains of NADPH oxidase p40phox and p47phox. J. Biol. Chem. 278, 14469-14479 (Pubitemid 36800000)
52. Stahelin, R. V., Long, F., Peter, B. J., Murray, D., De Camilli, P., McMahon, H. T., and Cho, W. (2003) Contrasting membrane interaction mechanisms of AP180 N-terminal homology (ANTH) and epsin N-terminal homology (ENTH) domains. J. Biol. Chem. 278, 28993-28999 (Pubitemid 36935811)
53. Manna, D., Albanese, A., Park, W. S., and Cho, W. (2007) Mechanistic basis of differential cellular responses of phosphatidylinositol 3,4-bispho-sphate- and phosphatidylinositol 3,4,5-trisphosphate-binding pleckstrin homology domains. J. Biol. Chem. 282, 32093-32105 (Pubitemid 350106465)
54. Demel, R. A., Geurts van Kessel, W. S., Zwaal, R. F., Roelofsen, B., and van Deenen, L. L. (1975) Relation between various phospholipase actions on human red cell membranes and the interfacial phospholipid pressure in monolayers. Biochim. Biophys. Acta 406, 97-107
55. Blume, A. (1979) A comparative study of the phase transitions of phospholipid bilayers and monolayers. Biochim. Biophys. Acta 557, 32-44
56. Marsh, D. (1996) Intrinsic curvature in normal and inverted lipid structures and in membranes. Biophys. J. 70, 2248-2255
57. Mim, C., Cui, H., Gawronski-Salerno, J. A., Frost, A., Lyman, E., Voth, G. A., and Unger, V. M. (2012) Structural basis of membrane bending by the N-BAR protein endophilin. Cell 149, 137-145
58. Mizuno, N., Jao, C. C., Langen, R., and Steven, A. C. (2010) Multiple modes of endophilin-mediated conversion of lipid vesicles into coated tubes: implications for synaptic endocytosis. J. Biol. Chem. 285, 23351-23358
59. Gortat, A., San-Roman, M. J., Vannier, C., and Schmidt, A. A. (2012) Single point mutation in Bin/Amphiphysin/Rvs (BAR) sequence of endophilin impairs dimerization, membrane shaping, and Src homology 3 domain-mediated partnership. J. Biol. Chem. 287, 4232-4247
60. Inoue, T., Heo, W. D., Grimley, J. S., Wandless, T. J., and Meyer, T. (2005) An inducible translocation strategy to rapidly activate and inhibit small GTPase signaling pathways. Nat. Methods 2, 415-418 (Pubitemid 40916559)
61. Varnai, P., Thyagarajan, B., Rohacs, T., and Balla, T. (2006) Rapidly inducible changes in phosphatidylinositol 4,5-bisphosphate levels influence multiple regulatory functions of the lipid in intact living cells. J. Cell Biol. 175, 377-382 (Pubitemid 44708062)
62. Yoon, Y., Lee, P. J., Kurilova, S., and Cho, W. (2011) In situ quantitative imaging of cellular lipids using molecular sensors. Nat. Chem. 3, 868-874
63. Yeung, T., Gilbert, G. E., Shi, J., Silvius, J., Kapus, A., and Grinstein, S. (2008) Membrane phosphatidylserine regulates surface charge and protein localization. Science 319, 210-213
64. Stahelin, R. V., Hwang, J. H., Kim, J. H., Park, Z. Y., Johnson, K. R., Obeid, L. M., and Cho, W. (2005) The mechanism of membrane targeting of human sphingosine kinase 1. J. Biol. Chem. 280, 43030-43038 (Pubitemid 43049268)
65. Stahelin, R. V., Rafter, J. D., Das, S., and Cho, W. (2003) The molecular basis of differential subcellular localization of C2 domains of protein kinase C-α and group IVa cytosolic phospholipase A2. J. Biol. Chem. 278, 12452-12460 (Pubitemid 36800232)
66. 3 in plasma membrane targeting of C2 domains. Molecular dynamics simulation, membrane binding, and cell translocation studies of the PKCα C2 domain. J. Biol. Chem. 283, 26047-26058
67. Leventis, P. A., and Grinstein, S. (2010) The distribution and function of phosphatidylserine in cellular membranes. Annu. Rev. Biophys. 39, 407-427
68. 2 lipids target proteins with polybasic clusters to the plasma membrane. Science 314, 1458-1461
69. Mulgrew-Nesbitt, A., Diraviyam, K., Wang, J., Singh, S., Murray, P., Li, Z., Rogers, L., Mirkovic, N., and Murray, D. (2006) The role of electrostatics in protein-membrane interactions. Biochim. Biophys. Acta 1761, 812-826 (Pubitemid 44332331)
70. Botelho, R. J., Teruel, M., Dierckman, R., Anderson, R., Wells, A., York, J. D., Meyer, T., and Grinstein, S. (2000) Localized biphasic changes in phosphatidylinositol-4,5-bisphosphate at sites of phagocytosis. J. Cell Biol. 151, 1353-1368
71. Garrenton, L. S., Stefan, C. J., McMurray, M. A., Emr, S. D., and Thorner, J. (2010) Pheromone-induced anisotropy in yeast plasma membrane phosphatidylinositol-4,5-bisphosphate distribution is required for MAPK signaling. Proc. Natl. Acad. Sci. U.S.A. 107, 11805-11810