Membrane Curvature Affects the Formation of α-Hemolysin Nanopores

ACS Chemical Biology

Volumn 10, Issue 7, 2015, Pages 1694-1701

  Fujii, Satoshi ^a   Matsuura, Tomoaki ^a,b   Yomo, Tetsuya ^a,b,c  

^a JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA HEMOLYSIN; LIPOSOME; BACTERIAL TOXIN; HEMOLYSIN; PROTEIN BINDING; STAPHYLOCOCCAL ALPHA-TOXIN;

ARTICLE; BIOCHEMICAL ANALYSIS; BIOLOGICAL FUNCTIONS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRON MICROSCOPY; EMULSION; ENDOPLASMIC RETICULUM; FLOW CYTOMETRY; IN VITRO STUDY; LIPID COMPOSITION; MEMBRANE BINDING; MEMBRANE CURVATURE; MEMBRANE STRUCTURE; MOLECULAR WEIGHT; MOLECULE; NANOPORE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN SYNTHESIS; RATE CONSTANT; RNA TRANSLATION; STAPHYLOCOCCUS AUREUS; SURFACE AREA; CHEMICAL STRUCTURE; CHEMISTRY; CYTOLOGY; METABOLISM; PROTEIN MULTIMERIZATION; ULTRASTRUCTURE;

STAPHYLOCOCCUS AUREUS;

BACTERIAL TOXINS; HEMOLYSIN PROTEINS; LIPOSOMES; MODELS, MOLECULAR; NANOPORES; PROTEIN BINDING; PROTEIN MULTIMERIZATION; STAPHYLOCOCCUS AUREUS;

EID: 84937159997     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/acschembio.5b00107     Document Type: Article

References (32)

1. Dowhan, W. (1997) Molecular basis for membrane phospholipid diversity: Why are there so many lipids? Annu. Rev. Biochem. 66, 199-232
2. Lee, A. G. (2003) Lipid-protein interactions in biological membranes: A structural perspective Biochim. Biophys. Acta 1612, 1-40
3. Vitrac, H., Bogdanov, M., and Dowhan, W. (2013) In vitro reconstitution of lipid-dependent dual topology and postassembly topological switching of a membrane protein Proc. Natl. Acad. Sci. U. S. A. 110, 9338-9343
4. Bogdanov, M. and Dowhan, W. (1995) Phosphatidylethanolamine Is Required for in-Vivo Function of the Membrane-Associated Lactose Permease of Escherichia-Coli J. Biol. Chem. 270, 732-739
5. 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
6. Bigay, J., Casella, J. F., Drin, G., Mesmin, B., and Antonny, B. (2005) ArfGAP1 responds to membrane curvature through the folding of a lipid packing sensor motif EMBO J. 24, 2244-2253
7. Antonny, B. (2010) Mechanisms of Membrane Curvature Sensing Annu. Rev. Biochem. 80, 101-123
8. Hatzakis, N. S., Bhatia, V. K., Larsen, J., Madsen, K. L., Bolinger, P. Y., Kunding, A. H., Castillo, J., Gether, U., Hedegard, P., and Stamou, D. (2009) How curved membranes recruit amphipathic helices and protein anchoring motifs Nat. Chem. Biol. 5, 835-841
9. Pujals, S., Miyamae, H., Afonin, S., Murayama, T., Hirose, H., Nakase, I., Taniuchi, K., Umeda, M., Sakamoto, K., Ulrich, A. S., and Futaki, S. (2013) Curvature engineering: Positive membrane curvature induced by epsin N-terminal peptide boosts internalization of octaarginine ACS Chem. Biol. 8, 1894-1899
10. Tabaei, S. R., Rabe, M., Zhdanov, V. P., Cho, N. J., and Hook, F. (2012) Single vesicle analysis reveals nanoscale membrane curvature selective pore formation in lipid membranes by an antiviral α-helical peptide Nano Lett. 12, 5719-5725
11. Jensen, M. B., Bhatia, V. K., Jao, C. C., Rasmussen, J. E., Pedersen, S. L., Jensen, K. J., Langen, R., and Stamou, D. (2011) Membrane curvature sensing by amphipathic helices: A single liposome study using alpha-synuclein and annexin B12 J. Biol. Chem. 286, 42603-42614
12. Rosenbaum, D. M., Rasmussen, S. G., and Kobilka, B. K. (2009) The structure and function of G-protein-coupled receptors Nature 459, 356-363
13. Yoshida, M., Muneyuki, E., and Hisabori, T. (2001) ATP synthase - a marvellous rotary engine of the cell Nat. Rev. Mol. Cell Biol. 2, 669-677
14. Arifuzzaman, M., Maeda, M., Itoh, A., Nishikata, K., Takita, C., Saito, R., Ara, T., Nakahigashi, K., Huang, H. C., Hirai, A., Tsuzuki, K., Nakamura, S., Altaf-Ul-Amin, M., Oshima, T., Baba, T., Yamamoto, N., Kawamura, T., Ioka-Nakamichi, T., Kitagawa, M., Tomita, M., Kanaya, S., Wada, C., and Mori, H. (2006) Large-scale identification of protein-protein interaction of Escherichia coli K-12 Genome Res. 16, 686-691
15. Stenberg, F., Chovanec, P., Maslen, S. L., Robinson, C. V., Ilag, L. L., von Heijne, G., and Daley, D. O. (2005) Protein complexes of the Escherichia coli cell envelope J. Biol. Chem. 280, 34409-34419
16. Gavin, A. C., Bosche, M., Krause, R., Grandi, P., Marzioch, M., Bauer, A., Schultz, J., Rick, J. M., Michon, A. M., Cruciat, C. M., Remor, M., Hofert, C., Schelder, M., Brajenovic, M., Ruffner, H., Merino, A., Klein, K., Hudak, M., Dickson, D., Rudi, T., Gnau, V., Bauch, A., Bastuck, S., Huhse, B., Leutwein, C., Heurtier, M. A., Copley, R. R., Edelmann, A., Querfurth, E., Rybin, V., Drewes, G., Raida, M., Bouwmeester, T., Bork, P., Seraphin, B., Kuster, B., Neubauer, G., and Superti-Furga, G. (2002) Functional organization of the yeast proteome by systematic analysis of protein complexes Nature 415, 141-147
17. Fujii, S., Matsuura, T., Sunami, T., Kazuta, Y., and Yomo, T. (2013) In vitro evolution of alpha-hemolysin using a liposome display Proc. Natl. Acad. Sci. U. S. A. 110, 16796-16801
18. Song, L., Hobaugh, M. R., Shustak, C., Cheley, S., Bayley, H., and Gouaux, J. E. (1996) Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore Science 274, 1859-1866
19. Nishimura, K., Hosoi, T., Sunami, T., Toyota, T., Fujinami, M., Oguma, K., Matsuura, T., Suzuki, H., and Yomo, T. (2009) Population analysis of structural properties of giant liposomes by flow cytometry Langmuir 25, 10439-10443
20. Nishimura, K., Matsuura, T., Sunami, T., Suzuki, H., and Yomo, T. (2012) Cell-free protein synthesis inside giant unilamellar vesicles analyzed by flow cytometry Langmuir 28, 8426-8432
21. Fujii, S., Matsuura, T., Sunami, T., Nishikawa, T., Kazuta, Y., and Yomo, T. (2014) Liposome display for in vitro selection and evolution of membrane proteins Nat. Protoc. 9, 1578-1591
22. Shimizu, Y., Inoue, A., Tomari, Y., Suzuki, T., Yokogawa, T., Nishikawa, K., and Ueda, T. (2001) Cell-free translation reconstituted with purified components Nat. Biotechnol. 19, 751-755
23. Walker, B., Krishnasastry, M., Zorn, L., and Bayley, H. (1992) Assembly of the oligomeric membrane pore formed by Staphylococcal alpha-hemolysin examined by truncation mutagenesis J. Biol. Chem. 267, 21782-21786
24. Valeva, A., Hellmann, N., Walev, I., Strand, D., Plate, M., Boukhallouk, F., Brack, A., Hanada, K., Decker, H., and Bhakdi, S. (2006) Evidence that clustered phosphocholine head groups serve as sites for binding and assembly of an oligomeric protein pore J. Biol. Chem. 281, 26014-26021
25. Palmer, M., Weller, U., Messner, M., and Bhakdi, S. (1993) Altered pore-forming properties of proteolytically nicked staphylococcal alpha-toxin J. Biol. Chem. 268, 11963-11967
26. Soga, H., Fujii, S., Yomo, T., Kato, Y., Watanabe, H., and Matsuura, T. (2013) In Vitro Membrane Protein Synthesis Inside Cell-Sized Vesicles Reveals the Dependence of Membrane Protein Integration on Vesicle Volume ACS Synth. Biol. 3, 372-379
27. Vermette, P. (2009) Liposome characterization by quartz crystal microbalance measurements and atomic force microscopy Methods Enzymol. 465, 43-73
28. Frederik, P. M. and Hubert, D. H. (2005) Cryoelectron microscopy of liposomes Methods Enzymol. 391, 431-448
29. Noireaux, V. and Libchaber, A. (2004) A vesicle bioreactor as a step toward an artificial cell assembly Proc. Natl. Acad. Sci. U. S. A. 101, 17669-17674
30. Yamada, A., Yamanaka, T., Hamada, T., Hase, M., Yoshikawa, K., and Baigl, D. (2006) Spontaneous transfer of phospholipid-coated oil-in-oil and water-in-oil micro-droplets through an oil/water interface Langmuir 22, 9824-9828
31. Pautot, S., Frisken, B. J., and Weitz, D. A. (2003) Production of Unilamellar Vesicles Using an Inverted Emulsion Langmuir 19, 2870-2879
32. Los, G. V., Encell, L. P., McDougall, M. G., Hartzell, D. D., Karassina, N., Zimprich, C., Wood, M. G., Learish, R., Ohana, R. F., Urh, M., Simpson, D., Mendez, J., Zimmerman, K., Otto, P., Vidugiris, G., Zhu, J., Darzins, A., Klaubert, D. H., Bulleit, R. F., and Wood, K. V. (2008) HaloTag: a novel protein labeling technology for cell imaging and protein analysis ACS Chem. Biol. 3, 373-382