Pore-forming toxins: Properties, diversity, and uses as tools to image sphingomyelin and ceramide phosphoethanolamine

Biochimica et Biophysica Acta - Biomembranes

Volumn 1858, Issue 3, 2016, Pages 576-592

  Yamaji Hasegawa, Akiko ^a   Hullin Matsuda, Françoise ^a,b   Greimel, Peter ^a   Kobayashi, Toshihide ^a,b  

^a RIKEN   (Japan)

^b UNIVERSITÉ LYON 1   (France)

Author keywords

Actinoporin; Aegerolysin; Equinatoxin; Lipid domains; Lipid imaging; Lysenin

Indexed keywords

ACTINOPORIN; AEGEROLYSIN; ANTIBODY; ASP HEMOLYSIN; AVT I TOXIN; CAISSAROLYSIN I; CERAMIDE PHOSPHOETHANOLAMINE; CLAMLYSIN; EQUINATOXIN; ERYLYSIN; FRAC TOXIN; GIGANTOXIN 4; HALT TOXIN; HCT TOXIN; LYSENIN; OSTREOLYSIN; PHOSPHOETHANOLAMINE; PLEUROTOLYSIN A; PLEUROTOLYSIN A2; PORE FORMING TOXIN; RTX TOXIN; SPHINGOMYELIN; SRC1 TOXIN; STICHOLYSIN I; STICHOLYSIN II; TERRELYSIN; TOXIC SUBSTANCE; TOXIN; UNCLASSIFIED DRUG; MOLECULAR PROBE; PORE FORMING CYTOTOXIC PROTEIN;

CELLULAR DISTRIBUTION; CHEMICAL ANALYSIS; CHEMICAL STRUCTURE; CONCENTRATION (PARAMETERS); IMAGE ANALYSIS; INSECT CELL; MAMMAL CELL; MASS SPECTROMETRY; MOLECULAR DYNAMICS; MOLECULAR IMAGING; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; REVIEW; SPECIES COMPOSITION; STRUCTURE ANALYSIS; ANIMAL; CHEMISTRY; HUMAN; INSECT; METABOLISM; MOLECULAR PROBE; PROCEDURES;

ANIMALS; HUMANS; INSECTS; MOLECULAR IMAGING; MOLECULAR PROBES; PORE FORMING CYTOTOXIC PROTEINS; SPHINGOMYELINS;

EID: 84956713837     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2015.10.012     Document Type: Review

References (206)

1. Y.A. Hannun, and L.M. Obeid Principles of bioactive lipid signalling: lessons from sphingolipids Nat. Rev. Mol. Cell Biol. 9 2008 139 150
2. K. Simons, and E. Ikonen Functional rafts in cell membranes Nature 387 1997 569 572
3. D. Lingwood, and K. Simons Lipid rafts as a membrane-organizing principle Science 327 2010 46 50
4. M. Skocaj, B. Bakrac, I. Krizaj, P. Macek, G. Anderluh, and K. Sepcic The sensing of membrane microdomains based on pore-forming toxins Curr. Med. Chem. 20 2013 491 501
5. N. Reig, and F.G. van der Goot About lipids and toxins FEBS Lett. 580 2006 5572 5579
6. Y. Ohno-Iwashita, Y. Shimada, M. Hayashi, M. Iwamoto, S. Iwashita, and M. Inomata Cholesterol-binding toxins and anti-cholesterol antibodies as structural probes for cholesterol localization Subcell. Biochem. 51 2010 597 621
7. D.A. Brown, and E. London Structure and function of sphingolipid- and cholesterol-rich membrane rafts J. Biol. Chem. 275 2000 17221 17224
8. K. Simons, and R. Ehehalt Cholesterol, lipid rafts, and disease J. Clin. Invest. 110 2002 597 603
9. D.A. Brown, and E. London Structure and origin of ordered lipid domains in biological membranes J. Membr. Biol. 164 1998 103 114
10. J.R. Silvius, D. del Giudice, and M. Lafleur Cholesterol at different bilayer concentrations can promote or antagonize lateral segregation of phospholipids of differing acyl chain length Biochemistry 35 1996 15198 15208
11. G. van Meer, D.R. Voelker, and G.W. Feigenson Membrane lipids: where they are and how they behave Nat. Rev. Mol. Cell Biol. 9 2008 112 124
12. B. Terova, R. Heczko, and J.P. Slotte On the importance of the phosphocholine methyl groups for sphingomyelin/cholesterol interactions in membranes: a study with ceramide phosphoethanolamine Biophys. J. 88 2005 2661 2669
13. K. Satouchi, K. Hirano, M. Sakaguchi, H. Takehara, and F. Matsuura Phospholipids from the free-living nematode Caenorhabditis elegans Lipids 28 1993 837 840
14. H.G. Elmendorf, and K. Haldar Plasmodium falciparum exports the Golgi marker sphingomyelin synthase into a tubovesicular network in the cytoplasm of mature erythrocytes J. Cell Biol. 124 1994 449 462
15. R.C. Dickson, C. Sumanasekera, and R.L. Lester Functions and metabolism of sphingolipids in Saccharomyces cerevisiae Prog. Lipid Res. 45 2006 447 465
16. L.J. Heung, C. Luberto, and M. Del Poeta Role of sphingolipids in microbial pathogenesis Infect. Immun. 74 2006 28 39
17. R.M. Dawson, N. Hemington, and D.B. Lindsay The phospholipids of the erythrocyte 'ghosts' of various species Biochem. J. 77 1960 226 230
18. R. Kraut Roles of sphingolipids in Drosophila development and disease J. Neurochem. 116 2011 764 778
19. A.M. Vacaru, J. van den Dikkenberg, P. Ternes, and J.C. Holthuis Ceramide phosphoethanolamine biosynthesis in Drosophila is mediated by a unique ethanolamine phosphotransferase in the Golgi lumen J. Biol. Chem. 288 2013 11520 11530
20. G. Simon, and G. Rouser Phospholipids of the sea anemone: quantitative distribution; absence of carbon-phosphorus linkages in glycerol phospholipids; structural elucidation of ceramide aminoethylphosphonate Lipids 2 1967 55 59
21. S.S. Sutterwala, F.F. Hsu, E.S. Sevova, K.J. Schwartz, K. Zhang, P. Key, J. Turk, S.M. Beverley, and J.D. Bangs Developmentally regulated sphingolipid synthesis in African trypanosomes Mol. Microbiol. 70 2008 281 296
22. A.H. Merrill Jr. Sphingolipid and glycosphingolipid metabolic pathways in the era of sphingolipidomics Chem. Rev. 111 2011 6387 6422
23. J.P. Slotte Biological functions of sphingomyelins Prog. Lipid Res. 52 2013 424 437
24. B. Ramstedt, P. Leppimaki, M. Axberg, and J.P. Slotte Analysis of natural and synthetic sphingomyelins using high-performance thin-layer chromatography Eur. J. Biochem. 266 1999 997 1002
25. R. Sandhoff Very long chain sphingolipids: tissue expression, function and synthesis FEBS Lett. 584 2010 1907 1913
26. E. Fahy, S. Subramaniam, H.A. Brown, C.K. Glass, A.H. Merrill Jr., R.C. Murphy, C.R. Raetz, D.W. Russell, Y. Seyama, W. Shaw, T. Shimizu, F. Spener, G. van Meer, M.S. VanNieuwenhze, S.H. White, J.L. Witztum, and E.A. Dennis A comprehensive classification system for lipids J. Lipid Res. 46 2005 839 861
27. E. Fahy, S. Subramaniam, R.C. Murphy, M. Nishijima, C.R. Raetz, T. Shimizu, F. Spener, G. van Meer, M.J. Wakelam, and E.A. Dennis Update of the LIPID MAPS comprehensive classification system for lipids J. Lipid Res. 50 2009 S9 14 (Suppl)
28. M. Carvalho, J.L. Sampaio, W. Palm, M. Brankatschk, S. Eaton, and A. Shevchenko Effects of diet and development on the Drosophila lipidome Mol. Syst. Biol. 8 2012 600
29. F.N. Hamada, M. Rosenzweig, K. Kang, S.R. Pulver, A. Ghezzi, T.J. Jegla, and P.A. Garrity An internal thermal sensor controlling temperature preference in Drosophila Nature 454 2008 217 220
30. D.T. Abeytunga, J.J. Glick, N.J. Gibson, L.A. Oland, A. Somogyi, V.H. Wysocki, and R. Polt Presence of unsaturated sphingomyelins and changes in their composition during the life cycle of the moth Manduca sexta J. Lipid Res. 45 2004 1221 1231
31. K. Huitema, J. van den Dikkenberg, J.F.H.M. Brouwers, and J.C.M. Holthuis Identification of a family of animal sphingomyelin synthases EMBO J. 23 2004 33 44
32. S. Yamaoka, M. Miyaji, T. Kitano, H. Umehara, and T. Okazaki Expression cloning of a human cDNA restoring sphingomyelin synthesis and cell growth in sphingomyelin synthase-defective lymphoid cells J. Biol. Chem. 279 2004 18688 18693
33. F.G. Tafesse, P. Ternes, and J.C. Holthuis The multigenic sphingomyelin synthase family J. Biol. Chem. 281 2006 29421 29425
34. M. Yano, K. Watanabe, T. Yamamoto, K. Ikeda, T. Senokuchi, M. Lu, T. Kadomatsu, H. Tsukano, M. Ikawa, M. Okabe, S. Yamaoka, T. Okazaki, H. Umehara, T. Gotoh, W.J. Song, K. Node, R. Taguchi, K. Yamagata, and Y. Oike Mitochondrial dysfunction and increased reactive oxygen species impair insulin secretion in sphingomyelin synthase 1-null mice J. Biol. Chem. 286 2011 3992 4002
35. Z. Li, Y. Fan, J. Liu, Y. Li, C. Huan, H.H. Bui, M.S. Kuo, T.S. Park, G. Cao, and X.C. Jiang Impact of sphingomyelin synthase 1 deficiency on sphingolipid metabolism and atherosclerosis in mice Arterioscler. Thromb. Vasc. Biol. 32 2012 1577 1584
36. M. Miyaji, Z.X. Jin, S. Yamaoka, R. Amakawa, S. Fukuhara, S.B. Sato, T. Kobayashi, N. Domae, T. Mimori, E.T. Bloom, T. Okazaki, and H. Umehara Role of membrane sphingomyelin and ceramide in platform formation for Fas-mediated apoptosis J. Exp. Med. 202 2005 249 259 (Epub 2005 Jul 2011)
37. S. Mitsutake, K. Zama, H. Yokota, T. Yoshida, M. Tanaka, M. Mitsui, M. Ikawa, M. Okabe, Y. Tanaka, T. Yamashita, H. Takemoto, T. Okazaki, K. Watanabe, and Y. Igarashi Dynamic modification of sphingomyelin in lipid microdomains controls development of obesity, fatty liver, and type 2 diabetes J. Biol. Chem. 286 2011 28544 28555
38. P. Ternes, J.F. Brouwers, J. van den Dikkenberg, and J.C. Holthuis Sphingomyelin synthase SMS2 displays dual activity as ceramide phosphoethanolamine synthase J. Lipid Res. 50 2009 2270 2277
39. T. Ding, I. Kabir, Y. Li, C. Lou, A. Yazdanyar, J. Xu, J. Dong, H. Zhou, T. Park, M. Boutjdir, Z. Li, and X.C. Jiang All members in the sphingomyelin synthase gene family have ceramide phosphoethanolamine synthase activity J. Lipid Res. 56 2015 537 545
40. A. Bickert, C. Ginkel, M. Kol, K. vom Dorp, H. Jastrow, J. Degen, R.L. Jacobs, D.E. Vance, E. Winterhager, X.C. Jiang, P. Dörmann, P. Somerharju, J.C. Holthuis, and K. Willecke Functional characterization of enzymes catalyzing ceramide phosphoethanolamine biosynthesis in mice J. Lipid Res. 56 2015 821 835
41. M. Malgat, A. Maurice, and J. Baraud Sphingomyelin and ceramide-phosphoethanolamine synthesis by microsomes and plasma membranes from rat liver and brain J. Lipid Res. 27 1986 251 260
42. D. Separovic, L. Semaan, A.L. Tarca, M.Y. Awad Maitah, K. Hanada, J. Bielawski, M. Villani, and C. Luberto Suppression of sphingomyelin synthase 1 by small interference RNA is associated with enhanced ceramide production and apoptosis after photodamage Exp. Cell Res. 314 2008 1860 1868
43. A.M. Vacaru, F.G. Tafesse, P. Ternes, V. Kondylis, M. Hermansson, J.F.H.M. Brouwers, P. Somerharju, C. Rabouille, and J.C.M. Holthuis Sphingomyelin synthase-related protein SMSr controls ceramide homeostasis in the ER J. Cell Biol. 185 2009 1013 1027
44. F.G. Tafesse, A.M. Vacaru, E.F. Bosma, M. Hermansson, A. Jain, A. Hilderink, P. Somerharju, and J.C.M. Holthuis Sphingomyelin synthase-related protein SMSr is a suppressor of ceramide-induced mitochondrial apoptosis J. Cell Sci. 127 2014 445 454
45. E.S. Sevova, M.A. Goren, K.J. Schwartz, F.F. Hsu, J. Turk, B.G. Fox, and J.D. Bangs Cell-free synthesis and functional characterization of sphingolipid synthases from parasitic trypanosomatid protozoa J. Biol. Chem. 285 2010 20580 20587
46. P.F. Devaux, and R. Morris Transmembrane asymmetry and lateral domains in biological membranes Traffic 5 2004 241 246
47. H.B. Bhat, R. Ishitsuka, T. Inaba, M. Murate, M. Abe, A. Makino, A. Kohyama-Koganeya, K. Nagao, A. Kurahashi, T. Kishimoto, M. Tahara, A. Yamano, K. Nagamune, Y. Hirabayashi, N. Juni, M. Umeda, F. Fujimori, K. Nishibori, A. Yamaji-Hasegawa, P. Greimel, and T. Kobayashi Evaluation of aegerolysins as novel tools to detect and visualize ceramide phosphoethanolamine, a major sphingolipid in invertebrates FASEB J. 29 2015 3920 3934
48. J. Peter Slotte Molecular properties of various structurally defined sphingomyelins - correlation of structure with function Prog. Lipid Res. 52 2013 206 219
49. K.A. Tanaka, K.G. Suzuki, Y.M. Shirai, S.T. Shibutani, M.S. Miyahara, H. Tsuboi, M. Yahara, A. Yoshimura, S. Mayor, T.K. Fujiwara, and A. Kusumi Membrane molecules mobile even after chemical fixation Nat. Methods 7 2010 865 866
50. T. Ando, N. Kodera, E. Takai, D. Maruyama, K. Saito, and A. Toda A high-speed atomic force microscope for studying biological macromolecules Proc. Natl. Acad. Sci. U. S. A. 98 2001 12468 12472
51. N. Yilmaz, T. Yamada, P. Greimel, T. Uchihashi, T. Ando, and T. Kobayashi Real-time visualization of assembling of a sphingomyelin-specific toxin on planar lipid membranes Biophys. J. 105 2013 1397 1405
52. R. Ishitsuka, A. Yamaji-Hasegawa, A. Makino, Y. Hirabayashi, and T. Kobayashi A lipid-specific toxin reveals heterogeneity of sphingomyelin-containing membranes Biophys. J. 86 2004 296 307
53. T. Kobayashi, A. Makino, and K. Ishii Vital staining of cells with fluorescent lipids, in: J. E. Cellis Cell Biology: A Laboratory Handbook 2006 Elsevier Burlington 139 145 (Chapter 20)
54. D.L. Marks, R.D. Singh, A. Choudhury, C.L. Wheatley, and R.E. Pagano Use of fluorescent sphingolipid analogs to study lipid transport along the endocytic pathway Methods 36 2005 186 195
55. P.F. Devaux, P. Fellmann, and P. Hervé Investigation on lipid asymmetry using lipid probes: comparison between spin-labeled lipids and fluorescent lipids Chem. Phys. Lipids 116 2002 115 134
56. M. Koval, and R.E. Pagano Lipid recycling between the plasma membrane and intracellular compartments: transport and metabolism of fluorescent sphingomyelin analogues in cultured fibroblasts J. Cell Biol. 108 1989 2169 2181
57. S. Mayor, J.F. Presley, and F.R. Maxfield Sorting of membrane components from endosomes and subsequent recycling to the cell surface occurs by a bulk flow process J. Cell Biol. 121 1993 1257 1269
58. M. Hao, and F.R. Maxfield Characterization of rapid membrane internalization and recycling J. Biol. Chem. 275 2000 15279 15286
59. M. Koval, and R.E. Pagano Sorting of an internalized plasma membrane lipid between recycling and degradative pathways in normal and Niemann-Pick, type A fibroblasts J. Cell Biol. 111 1990 429 442
60. R.E. Pagano, M.A. Sepanski, and O.C. Martin Molecular trapping of a fluorescent ceramide analogue at the Golgi apparatus of fixed cells: interaction with endogenous lipids provides a trans-Golgi marker for both light and electron microscopy J. Cell Biol. 109 1989 2067 2079
61. R.E. Pagano, V. Puri, M. Dominguez, and D.L. Marks Membrane traffic in sphingolipid storage diseases Traffic 1 2000 807 815
62. N.G. Lipsky, and R.E. Pagano A vital stain for the Golgi apparatus Science 228 1985 745 747
63. N.G. Lipsky, and R.E. Pagano Sphingolipid metabolism in cultured fibroblasts: microscopic and biochemical studies employing a fluorescent ceramide analogue Proc. Natl. Acad. Sci. U. S. A. 80 1983 2608 2612
64. A. Chattopadhyay Chemistry and biology of N-(7-nitrobenz-2-oxa-1,3-diazol-4-yl)-labeled lipids: fluorescent probes of biological and model membranes Chem. Phys. Lipids 53 1990 1 15
65. C. Nusshold, A. Uellen, E. Bernhart, A. Hammer, S. Damm, A. Wintersperger, H. Reicher, A. Hermetter, E. Malle, and W. Sattler Endocytosis and intracellular processing of BODIPY-sphingomyelin by murine CATH.a neurons Biochim. Biophys. Acta 1831 2013 1665 1678
66. R.E. Pagano, O.C. Martin, H.C. Kang, and R.P. Haugland A novel fluorescent ceramide analogue for studying membrane traffic in animal cells: accumulation at the Golgi apparatus results in altered spectral properties of the sphingolipid precursor J. Cell Biol. 113 1991 1267 1279
67. R.E. Pagano, R. Watanabe, C. Wheatley, and M. Dominguez Applications of BODIPY-sphingolipid analogs to study lipid traffic and metabolism in cells Methods Enzymol. 312 2000 523 534
68. I.D. Johnson, H.C. Kang, and R.P. Haugland Fluorescent membrane probes incorporating dipyrrometheneboron difluoride fluorophores Anal. Biochem. 198 1991 228 237
69. T. Makiyama, H. Nakamura, N. Nagasaka, H. Yamashita, T. Honda, N. Yamaguchi, A. Nishida, and T. Murayama Trafficking of acetyl-C16-ceramide-NBD with long-term stability and no cytotoxicity into the Golgi complex Traffic 16 2015 476 492
70. M. Koivusalo, J. Alvesalo, J.A. Virtanen, and P. Somerharju Partitioning of pyrene-labeled phospho- and sphingolipids between ordered and disordered bilayer domains Biophys. J. 86 2004 923 935
71. M. Koivusalo, M. Jansen, P. Somerharju, and E. Ikonen Endocytic trafficking of sphingomyelin depends on its acyl chain length Mol. Biol. Cell 18 2007 5113 5123
72. H.C. Kolb, M.G. Finn, and K.B. Sharpless Click chemistry: diverse chemical function from a few good reactions Angew. Chem. Int. Ed. Engl. 40 2001 2004 2021
73. A. Gaebler, R. Milan, L. Straub, D. Hoelper, L. Kuerschner, and C. Thiele Alkyne lipids as substrates for click chemistry-based in vitro enzymatic assays J. Lipid Res. 54 2013 2282 2290
74. P. Haberkant, and J.C.M. Holthuis Fat & fabulous: bifunctional lipids in the spotlight Biochim. Biophys. Acta 1841 2014 1022 1030
75. A.B. Neef, and C. Schultz Selective fluorescence labeling of lipids in living cells Angew. Chem. Int. Ed. Engl. 48 2009 1498 1500
76. C.Y. Jao, M. Roth, R. Welti, and A. Salic Metabolic labeling and direct imaging of choline phospholipids in vivo Proc. Natl. Acad. Sci. U. S. A. 106 2009 15332 15337
77. S. Iyoshi, J. Cheng, T. Tatematsu, S. Takatori, M. Taki, Y. Yamamoto, A. Salic, and T. Fujimoto Asymmetrical distribution of choline phospholipids revealed by click chemistry and freeze-fracture electron microscopy ACS Chem. Biol. 9 2014 2217 2222
78. M. Seigneuret, and P.F. Devaux ATP-dependent asymmetric distribution of spin-labeled phospholipids in the erythrocyte membrane: relation to shape changes Proc. Natl. Acad. Sci. U. S. A. 81 1984 3751 3755
79. A. Zachowski, P. Fellman, and P.F. Devaux Absence of transbilayer diffusion of spin-labeled sphingomyelin on human erythrocytes. Comparison with the diffusion of several spin-labeled glycerophospholipids Biochim. Biophys. Acta 815 1985 510 514
80. I. Lopez-Montero, N. Rodriguez, S. Cribier, A. Pohl, M. Velez, and P.F. Devaux Rapid transbilayer movement of ceramides in phospholipid vesicles and in human erythrocytes J. Biol. Chem. 280 2005 25811 25819
81. F. Ogushi, R. Ishitsuka, T. Kobayashi, and Y. Sugita Rapid flip-flop motions of diacylglycerol and ceramide in phospholipid bilayers Chem. Phys. Lett. 522 2012 96 102
82. H. Mizuno, M. Abe, P. Dedecker, A. Makino, S. Rocha, Y. Ohno-Iwashita, J. Hofkens, T. Kobayashi, and A. Miyawaki Fluorescent probes for superresolution imaging of lipid domains on the plasma membrane Chem. Sci. 2 2011 1548 1553
83. M. Abe, A. Makino, F. Hullin-Matsuda, K. Kamijo, Y. Ohno-Iwashita, K. Hanada, H. Mizuno, A. Miyawaki, and T. Kobayashi A role for sphingomyelin-rich lipid domains in the accumulation of phosphatidylinositol-4,5-bisphosphate to the cleavage furrow during cytokinesis Mol. Cell. Biol. 32 2012 1396 1407
84. S.G. Boxer, M.L. Kraft, and P.K. Weber Advances in imaging secondary ion mass spectrometry for biological samples Annu. Rev. Biophys. 38 2009 53 74
85. Y. Sugiura, and M. Setou Matrix-assisted laser desorption/ionization and nanoparticle-based imaging mass spectrometry for small metabolites: a practical protocol Methods Mol. Biol. 656 2010 173 195
86. E.R. Amstalden van Hove, D.F. Smith, and R.M. Heeren A concise review of mass spectrometry imaging J. Chromatogr. A 1217 2010 3946 3954
87. E.E. Jones, S. Dworski, D. Canals, J. Casas, G. Fabrias, D. Schoenling, T. Levade, C. Denlinger, Y.A. Hannun, J.A. Medin, and R.R. Drake On-tissue localization of ceramides and other sphingolipids by MALDI mass spectrometry imaging Anal. Chem. 86 2014 8303 8311
88. L. Muller, A. Kailas, S.N. Jackson, A. Roux, D.C. Barbacci, J.A. Schultz, C.D. Balaban, and A.S. Woods Lipid imaging within the normal rat kidney using silver nanoparticles by matrix-assisted laser desorption/ionization mass spectrometry Kidney Int. 88 2015 186 192
89. J.F. Frisz, K. Lou, H.A. Klitzing, W.P. Hanafin, V. Lizunov, R.L. Wilson, K.J. Carpenter, R. Kim, I.D. Hutcheon, J. Zimmerberg, P.K. Weber, and M.L. Kraft Direct chemical evidence for sphingolipid domains in the plasma membranes of fibroblasts Proc. Natl. Acad. Sci. U. S. A. 110 2013 E613 E622
90. K. Fujimoto, M. Umeda, and T. Fujimoto Transmembrane phospholipid distribution revealed by freeze-fracture replica labeling J. Cell Sci. 109 Pt 10 1996 2453 2460
91. M. Murate, M. Abe, K. Kasahara, K. Iwabuchi, M. Umeda, and T. Kobayashi Transbilayer distribution of lipids at nano scale J. Cell Sci. 128 2015 1627 1638
92. D. Toomre, and J. Bewersdorf A new wave of cellular imaging Annu. Rev. Cell Dev. Biol. 26 2010 285 314
93. M. Fernandez-Suarez, and A.Y. Ting Fluorescent probes for super-resolution imaging in living cells Nat. Rev. Mol. Cell Biol. 9 2008 929 943
94. M. Maekawa, and G.D. Fairn Molecular probes to visualize the location, organization and dynamics of lipids J. Cell Sci. 127 2014 4801 4812
95. S. Furuya, J. Mitoma, A. Makino, and Y. Hirabayashi Ceramide and its interconvertible metabolite sphingosine function as indispensable lipid factors involved in survival and dendritic differentiation of cerebellar Purkinje cells J. Neurochem. 71 1998 366 377
96. K. Hirota, K. Momoeda, K. Ono, K. Hanaoka, K. Horikawa, K. Okumura, and M. Iwamori Alteration in the reactivity of sphingomyelin in mitogen-stimulated lymphocytes J. Biochem. 118 1995 4 8
97. M. Iwamori, K. Hirota, T. Utsuki, K. Momoeda, K. Ono, Y. Tsuchida, K. Okumura, and K. Hanaoka Sensitive method for the determination of pulmonary surfactant phospholipid/sphingomyelin ratio in human amniotic fluids for the diagnosis of respiratory distress syndrome by thin-layer chromatography-immunostaining Anal. Biochem. 238 1996 29 33
98. L.A. Cowart, Z. Szulc, A. Bielawska, and Y.A. Hannun Structural determinants of sphingolipid recognition by commercially available anti-ceramide antibodies J. Lipid Res. 43 2002 2042 2048 10.1194/jlr.M200241-JLR200
99. K. Krishnamurthy, S. Dasgupta, and E. Bieberich Development and characterization of a novel anti-ceramide antibody J. Lipid Res. 48 2007 968 975
100. M. Kawase, M. Watanabe, T. Kondo, T. Yabu, Y. Taguchi, H. Umehara, T. Uchiyama, K. Mizuno, and T. Okazaki Increase of ceramide in adriamycin-induced HL-60 cell apoptosis: detection by a novel anti-ceramide antibody Biochim. Biophys. Acta 1584 2002 104 114
101. J. Rotolo, B. Stancevic, J. Zhang, G. Hua, J. Fuller, X. Yin, A. Haimovitz-Friedman, K. Kim, M. Qian, xF. Card, M. Vila, Z. Fuks, R. Pasqualini, W. Arap, and R. Kolesnick Anti-ceramide antibody prevents the radiation gastrointestinal syndrome in mice J. Clin. Invest. 122 2012 1786 1790
102. M. Bischofberger, M.R. Gonzalez, and F.G. van der Goot Membrane injury by pore-forming proteins Curr. Opin. Cell Biol. 21 2009 589 595
103. A. Yamaji, Y. Sekizawa, K. Emoto, H. Sakuraba, K. Inoue, H. Kobayashi, and M. Umeda Lysenin, a novel sphingomyelin-specific binding protein J. Biol. Chem. 273 1998 5300 5306
104. B. Bakrac, I. Gutierrez-Aguirre, Z. Podlesek, A.F. Sonnen, R.J. Gilbert, P. Macek, J.H. Lakey, and G. Anderluh Molecular determinants of sphingomyelin specificity of a eukaryotic pore-forming toxin J. Biol. Chem. 283 2008 18665 18677
105. S. Berne, L. Lah, and K. Sepcic Aegerolysins: structure, function, and putative biological role Protein Sci. 18 2009 694 706
106. E. Kiyokawa, A. Makino, K. Ishii, N. Otsuka, A. Yamaji-Hasegawa, and T. Kobayashi Recognition of sphingomyelin by lysenin and lysenin-related proteins Biochemistry 43 2004 9766 9773
107. L. De Colibus, A.F. Sonnen, K.J. Morris, C.A. Siebert, P. Abrusci, J. Plitzko, V. Hodnik, M. Leippe, E. Volpi, G. Anderluh, and R.J. Gilbert Structures of lysenin reveal a shared evolutionary origin for pore-forming proteins and its mode of sphingomyelin recognition Structure 20 2012 1498 1507
108. E. Betzig, G.H. Patterson, R. Sougrat, O.W. Lindwasser, S. Olenych, J.S. Bonifacino, M.W. Davidson, J. Lippincott-Schwartz, and H.F. Hess Imaging intracellular fluorescent proteins at nanometer resolution Science 313 2006 1642 1645
109. S. van de Linde, A. Loschberger, T. Klein, M. Heidbreder, S. Wolter, M. Heilemann, and M. Sauer Direct stochastic optical reconstruction microscopy with standard fluorescent probes Nat. Protoc. 6 2011 991 1009
110. K.I. Willig, R.R. Kellner, R. Medda, B. Hein, S. Jakobs, and S.W. Hell Nanoscale resolution in GFP-based microscopy Nat. Methods 3 2006 721 723
111. M. Carquin, H. Pollet, M. Veiga-da-Cunha, A. Cominelli, P. Van Der Smissen, F. N'Kuli, H. Emonard, P. Henriet, H. Mizuno, P.J. Courtoy, and D. Tyteca Endogenous sphingomyelin segregates into submicrometric domains in the living erythrocyte membrane J. Lipid Res. 55 2014 1331 1342
112. S. Hebbar, E. Lee, M. Manna, S. Steinert, G.S. Kumar, M. Wenk, T. Wohland, and R. Kraut A fluorescent sphingolipid binding domain peptide probe interacts with sphingolipids and cholesterol-dependent raft domains J. Lipid Res. 49 2008 1077 1089 10.1194/jlr.M700543-JLR200
113. M.P. Clausen, and B.C. Lagerholm The probe rules in single particle tracking Curr. Protein Pept. Sci. 12 2011 699 713
114. E. Kiyokawa, T. Baba, N. Otsuka, A. Makino, S. Ohno, and T. Kobayashi Spatial and functional heterogeneity of sphingolipid-rich membrane domains J. Biol. Chem. 280 2005 24072 24084 (Epub 22005 Apr 24019)
115. A. Makino, M. Abe, M. Murate, T. Inaba, N. Yilmaz, F. Hullin-Matsuda, T. Kishimoto, N.L. Schieber, T. Taguchi, H. Arai, G. Anderluh, R.G. Parton, and T. Kobayashi Visualization of the heterogeneous membrane distribution of sphingomyelin associated with cytokinesis, cell polarity, and sphingolipidosis FASEB J. 29 2015 477 493
116. K. Hanada, T. Hara, M. Fukasawa, A. Yamaji, M. Umeda, and M. Nishijima Mammalian cell mutants resistant to a sphingomyelin-directed cytolysin. Genetic and biochemical evidence for complex formation of the LCB1 protein with the LCB2 protein for serine palmitoyltransferase J. Biol. Chem. 273 1998 33787 33794
117. F. Hullin-Matsuda, N. Tomishige, S. Sakai, R. Ishitsuka, K. Ishii, A. Makino, P. Greimel, M. Abe, E.L. Laviad, M. Lagarde, H. Vidal, T. Saito, H. Osada, K. Hanada, A.H. Futerman, and T. Kobayashi Limonoid compounds inhibit sphingomyelin biosynthesis by preventing CERT protein-dependent extraction of ceramides from the endoplasmic reticulum J. Biol. Chem. 287 2012 24397 24411
118. Q. Hong, I. Gutierrez-Aguirre, A. Barlic, P. Malovrh, K. Kristan, Z. Podlesek, P. Macek, D. Turk, J.M. Gonzalez-Manas, J.H. Lakey, and G. Anderluh Two-step membrane binding by equinatoxin II, a pore-forming toxin from the sea anemone, involves an exposed aromatic cluster and a flexible helix J. Biol. Chem. 277 2002 41916 41924
119. S. Garcia-Linares, R. Richmond, M.F. Garcia-Mayoral, N. Bustamante, M. Bruix, J.G. Gavilanes, and A. Martinez-Del-Pozo The sea anemone actinoporin (Arg-Gly-Asp) conserved motif is involved in maintaining the competent oligomerization state of these pore-forming toxins FEBS J. 281 2014 1465 1478
120. M.G. Hinds, W. Zhang, G. Anderluh, P.E. Hansen, and R.S. Norton Solution structure of the eukaryotic pore-forming cytolysin equinatoxin II: implications for pore formation J. Mol. Biol. 315 2002 1219 1229
121. J.M. Mancheno, J. Martin-Benito, M. Martinez-Ripoll, J.G. Gavilanes, and J.A. Hermoso Crystal and electron microscopy structures of sticholysin II actinoporin reveal insights into the mechanism of membrane pore formation Structure 11 2003 1319 1328
122. A. Athanasiadis, G. Anderluh, P. Macek, and D. Turk Crystal structure of the soluble form of equinatoxin II, a pore-forming toxin from the sea anemone Actinia equina Structure 9 2001 341 346
123. A.E. Mechaly, A. Bellomio, K. Morante, J.M. Gonzalez-Manas, and D.M. Guerin Crystallization and preliminary crystallographic analysis of fragaceatoxin C, a pore-forming toxin from the sea anemone Actinia fragacea Acta Crystallogr. Sect. F: Struct. Biol. Cryst. Commun. 65 2009 357 360
124. M.E. Lanio, V. Morera, C. Alvarez, M. Tejuca, T. Gomez, F. Pazos, V. Besada, D. Martinez, V. Huerta, G. Padron, and M. de los Angeles Chavez Purification and characterization of two hemolysins from Stichodactyla helianthus Toxicon 39 2001 187 194
125. D. Martinez, A.M. Campos, F. Pazos, C. Alvarez, M.E. Lanio, F. Casallanovo, S. Schreier, R.K. Salinas, C. Vergara, and E. Lissi Properties of St I and St II, two isotoxins isolated from Stichodactyla helianthus: a comparison Toxicon 39 2001 1547 1560
126. V. Huerta, V. Morera, Y. Guanche, G. Chinea, L.J. Gonzalez, L. Betancourt, D. Martinez, C. Alvarez, M.E. Lanio, and V. Besada Primary structure of two cytolysin isoforms from Stichodactyla helianthus differing in their hemolytic activity Toxicon 39 2001 1253 1256
127. U. Ros, L. Pedrera, D. Diaz, J.C. Karam, T.P. Sudbrack, P.A. Valiente, D. MartInez, E.M. Cilli, F. Pazos, R. Itri, M.E. Lanio, S. Schreier, and C. Avarez The membranotropic activity of N-terminal peptides from the pore-forming proteins sticholysin I and II is modulated by hydrophobic and electrostatic interactions as well as lipid composition J. Biosci. 36 2011 781 791
128. I.F. Pazos, D. Martinez, M. Tejuca, A. Valle, A. del Pozo, C. Alvarez, M.E. Lanio, and E.A. Lissi Comparison of pore-forming ability in membranes of a native and a recombinant variant of Sticholysin II from Stichodactyla helianthus Toxicon 42 2003 571 578
129. U. Ros, A.L. Souto, F.J. de Oliveira, E. Crusca Jr., F. Pazos, E.M. Cilli, M.E. Lanio, S. Schreier, and C. Alvarez Functional and topological studies with Trp-containing analogs of the peptide StII1-30 derived from the N-terminus of the pore forming toxin sticholysin II: contribution to understand its orientation in membrane Biopolymers 100 2013 337 346
130. V. de los Rios, J.M. Mancheno, A. Martinez del Pozo, C. Alfonso, G. Rivas, M. Onaderra, and J.G. Gavilanes Sticholysin II, a cytolysin from the sea anemone Stichodactyla helianthus, is a monomer-tetramer associating protein FEBS Lett. 455 1999 27 30
131. D. Martinez, A. Otero, C. Alvarez, F. Pazos, M. Tejuca, M.E. Lanio, I. Gutierrez-Aguirre, A. Barlic, I. Iloro, J.L. Arrondo, J.M. Gonzalez-Manas, and E. Lissi Effect of sphingomyelin and cholesterol on the interaction of St II with lipidic interfaces Toxicon 49 2007 68 81
132. V. de los Rios, J.M. Mancheno, M.E. Lanio, M. Onaderra, and J.G. Gavilanes Mechanism of the leakage induced on lipid model membranes by the hemolytic protein sticholysin II from the sea anemone Stichodactyla helianthus Eur. J. Biochem. 252 1998 284 289
133. M. Tejuca, M. Dalla Serra, C. Potrich, C. Alvarez, and G. Menestrina Sizing the radius of the pore formed in erythrocytes and lipid vesicles by the toxin sticholysin I from the sea anemone Stichodactyla helianthus J. Membr. Biol. 183 2001 125 135
134. M. Tejuca, M.D. Serra, M. Ferreras, M.E. Lanio, and G. Menestrina Mechanism of membrane permeabilization by sticholysin I, a cytolysin isolated from the venom of the sea anemone Stichodactyla helianthus Biochemistry 35 1996 14947 14957
135. S. Garcia-Linares, I. Alm, T. Maula, J.G. Gavilanes, J.P. Slotte, and A. Martinez-Del-Pozo The effect of cholesterol on the long-range network of interactions established among sea anemone Sticholysin II residues at the water-membrane interface Mar. Drugs 13 2015 1647 1665
136. P. Macek, and D. Lebez Isolation and characterization of three lethal and hemolytic toxins from the sea anemone Actinia equina L Toxicon 26 1988 441 451
137. G. Anderluh, J. Pungercar, B. Strukelj, P. Macek, and F. Gubensek Cloning, sequencing, and expression of equinatoxin II Biochem. Biophys. Res. Commun. 220 1996 437 442
138. E. Glasser, T. Rachamim, D. Aharonovich, and D. Sher Hydra actinoporin-like toxin-1, an unusual hemolysin from the nematocyst venom of Hydra magnipapillata which belongs to an extended gene family Toxicon 91 2014 103 113
139. G. Belmonte, C. Pederzolli, P. Macek, and G. Menestrina Pore formation by the sea anemone cytolysin equinatoxin II in red blood cells and model lipid membranes J. Membr. Biol. 131 1993 11 22
140. M.A. Baker, N. Rojko, B. Cronin, G. Anderluh, and M.I. Wallace Photobleaching reveals heterogeneous stoichiometry for equinatoxin II oligomers Chembiochem 15 2014 2139 2145
141. Y. Subburaj, U. Ros, E. Hermann, R. Tong, and A.J. Garcia-Saez Toxicity of an alpha-pore-forming toxin depends on the assembly mechanism on the target membrane as revealed by single molecule imaging J. Biol. Chem. 290 2015 4856 4865
142. G. Anderluh, J. Pungercar, I. Krizaj, B. Strukelj, F. Gubensek, and P. Macek N-terminal truncation mutagenesis of equinatoxin II, a pore-forming protein from the sea anemone Actinia equina Protein Eng. 10 1997 751 755
143. G. Anderluh, A. Barlic, I. Krizaj, G. Menestrina, F. Gubensek, and P. Macek Avidin-FITC topological studies with three cysteine mutants of equinatoxin II, a sea anemone pore-forming protein Biochem. Biophys. Res. Commun. 242 1998 187 190
144. G. Anderluh, A. Barlic, Z. Podlesek, P. Macek, J. Pungercar, F. Gubensek, M.L. Zecchini, M.D. Serra, and G. Menestrina Cysteine-scanning mutagenesis of an eukaryotic pore-forming toxin from sea anemone: topology in lipid membranes Eur. J. Biochem. 263 1999 128 136
145. G. Anderluh, A. Barlic, C. Potrich, P. Macek, and G. Menestrina Lysine 77 is a key residue in aggregation of equinatoxin II, a pore-forming toxin from sea anemone Actinia equina J. Membr. Biol. 173 2000 47 55
146. P. Malovrh, G. Viero, M.D. Serra, Z. Podlesek, J.H. Lakey, P. Macek, G. Menestrina, and G. Anderluh A novel mechanism of pore formation: membrane penetration by the N-terminal amphipathic region of equinatoxin J. Biol. Chem. 278 2003 22678 22685
147. A. Barlic, I. Gutierrez-Aguirre, J.M. Caaveiro, A. Cruz, M.B. Ruiz-Arguello, J. Perez-Gil, and J.M. Gonzalez-Manas Lipid phase coexistence favors membrane insertion of equinatoxin-II, a pore-forming toxin from Actinia equina J. Biol. Chem. 279 2004 34209 34216
148. P. Macek, M. Zecchini, C. Pederzolli, M. Dalla Serra, and G. Menestrina Intrinsic tryptophan fluorescence of equinatoxin II, a pore-forming polypeptide from the sea anemone Actinia equina L, monitors its interaction with lipid membranes Eur. J. Biochem. 234 1995 329 335
149. J.M. Caaveiro, I. Echabe, I. Gutierrez-Aguirre, J.L. Nieva, J.L. Arrondo, and J.M. Gonzalez-Manas Differential interaction of equinatoxin II with model membranes in response to lipid composition Biophys. J. 80 2001 1343 1353
150. A. Drechsler, G. Anderluh, R.S. Norton, and F. Separovic Solid-state NMR study of membrane interactions of the pore-forming cytolysin, equinatoxin II Biochim. Biophys. Acta 1798 2010 244 251
151. N. Rojko, B. Cronin, J.S. Danial, M.A. Baker, G. Anderluh, and M.I. Wallace Imaging the lipid-phase-dependent pore formation of equinatoxin II in droplet interface bilayers Biophys. J. 106 2014 1630 1637
152. A. Bellomio, K. Morante, A. Barlic, I. Gutierrez-Aguirre, A.R. Viguera, and J.M. Gonzalez-Manas Purification, cloning and characterization of fragaceatoxin C, a novel actinoporin from the sea anemone Actinia fragacea Toxicon 54 2009 869 880
153. K. Morante, J.M. Caaveiro, K. Tanaka, J.M. Gonzalez-Manas, and K. Tsumoto A pore-forming toxin requires a specific residue for its activity in membranes with particular physicochemical properties J. Biol. Chem. 290 2015 10850 10861
154. X. Jiang, H. Chen, W. Yang, Y. Liu, W. Liu, J. Wei, H. Tu, X. Xie, L. Wang, and A. Xu Functional expression and characterization of an acidic actinoporin from sea anemone Sagartia rosea Biochem. Biophys. Res. Commun. 312 2003 562 570
155. M.M. Monastyrnaya, T.A. Zykova, O.V. Apalikova, T.V. Shwets, and E.P. Kozlovskaya Biologically active polypeptides from the tropical sea anemone Radianthus macrodactylus Toxicon 40 2002 1197 1217
156. E.V. Klyshko, M.P. Issaeva, M.M. Monastyrnaya, A.P. Il'yna, K.V. Guzev, T.I. Vakorina, P.S. Dmitrenok, T.A. Zykova, and E.P. Kozlovskaya Isolation, properties and partial amino acid sequence of a new actinoporin from the sea anemone Radianthus macrodactylus Toxicon 44 2004 315 324
157. E.S. Tkacheva, E.V. Leychenko, M.M. Monastyrnaya, M.P. Issaeva, E.A. Zelepuga, S.D. Anastuk, P.S. Dmitrenok, and E.P. Kozlovskaya New actinoporins from sea anemone Heteractis crispa: cloning and functional expression Biochemistry (Mosc) 76 2011 1131 1139
158. E.V. Leichenko, M.M. Monastirnaya, E.A. Zelepuga, E.S. Tkacheva, M.P. Isaeva, G.N. Likhatskaya, S.D. Anastyuk, and E.P. Kozlovskaya Hct-a is a new actinoporin family from the Heteractis crispa sea anemone Acta Nat. 6 2014 89 98
159. G. Uechi, H. Toma, T. Arakawa, and Y. Sato Biochemical and physiological analyses of a hemolytic toxin isolated from a sea anemone Actineria villosa Toxicon 45 2005 761 766
160. J.S. de Oliveira, A.J. Zaharenko, J.C. de Freitas, K. Konno, S.A. de Andrade, F.C. Portaro, M. Richardson, O.A. Sant'anna, and D.V. Tambourgi Caissarolysin I (Bcs I), a new hemolytic toxin from the Brazilian sea anemone Bunodosoma caissarum: purification and biological characterization Biochim. Biophys. Acta 1760 2006 453 461
161. B. Hu, W. Guo, L.H. Wang, J.G. Wang, X.Y. Liu, and B.H. Jiao Purification and characterization of gigantoxin-4, a new actinoporin from the sea anemone Stichodactyla gigantea Int. J. Biol. Sci. 7 2011 729 739
162. Y.J. Liew, W.T. Soh, W.F. Jiemy, and J.S. Hwang Mutagenesis and functional analysis of the pore-forming toxin HALT-1 from Hydra magnipapillata Toxins (Basel) 7 2015 407 422
163. T. Takara, T. Nakagawa, M. Isobe, N. Okino, S. Ichinose, A. Omori, and M. Ito Purification, molecular cloning, and application of a novel sphingomyelin-binding protein (clamlysin) from the brackishwater clam, Corbicula japonica Biochim. Biophys. Acta 1811 2011 323 332
164. J. Alegre-Cebollada, I. Rodriguez-Crespo, J.G. Gavilanes, and A.M. del Pozo Detergent-resistant membranes are platforms for actinoporin pore-forming activity on intact cells FEBS J. 273 2006 863 871
165. P.S. Garcia, G. Chieppa, A. Desideri, S. Cannata, E. Romano, P. Luly, and S. Rufini Sticholysin II: a pore-forming toxin as a probe to recognize sphingomyelin in artificial and cellular membranes Toxicon 60 2012 724 733
166. B. Bakrac, A. Kladnik, P. Macek, G. McHaffie, A. Werner, J.H. Lakey, and G. Anderluh A toxin-based probe reveals cytoplasmic exposure of Golgi sphingomyelin J. Biol. Chem. 285 2010 22186 22195
167. M.T. Fernandez Espinar, and J. Labarere Cloning and sequencing of the Aa-Pri1 gene specifically expressed during fruiting initiation in the edible mushroom Agrocybe aegerita, and analysis of the predicted amino-acid sequence Curr. Genet. 32 1997 420 424
168. S. Berne, I. Krizaj, F. Pohleven, T. Turk, P. Macek, and K. Sepcic Pleurotus and Agrocybe hemolysins, new proteins hypothetically involved in fungal fruiting Biochim. Biophys. Acta 1570 2002 153 159
169. M. Novak, N. Krasevec, M. Skocaj, P. Macek, G. Anderluh, and K. Sepcic Fungal aegerolysin-like proteins: distribution, activities, and applications Appl. Microbiol. Biotechnol. 99 2015 601 610
170. O. Sakaguchi, H. Shimada, and K. Yokota Proceedings: purification and characteristics of hemolytic toxin from Aspergillus fumigatus Jpn. J. Med. Sci. Biol. 28 1975 328 331
171. K. Ebina, H. Sakagami, K. Yokota, and H. Kondo Cloning and nucleotide sequence of cDNA encoding Asp-hemolysin from Aspergillus fumigatus Biochim. Biophys. Acta 1219 1994 148 150
172. Y. Fukuchi, Y. Kudo, T. Kumagai, K. Ebina, and K. Yokota Oxidized low density lipoprotein inhibits the hemolytic activity of Asp-hemolysin from Aspergillus fumigatus FEMS Microbiol. Lett. 167 1998 275 280
173. Y. Kudo, Y. Fukuchi, T. Kumagai, K. Ebina, and K. Yokota Oxidized low-density lipoprotein-binding specificity of Asp-hemolysin from Aspergillus fumigatus Biochim. Biophys. Acta 1568 2001 183 188
174. Y. Kudo, T. Ootani, T. Kumagai, Y. Fukuchi, K. Ebin, and K. Yokota A novel oxidized low-density lipoprotein-binding protein, Asp-hemolysin, recognizes lysophosphatidylcholine Biol. Pharm. Bull. 25 2002 787 790
175. A.P. Nayak, F.M. Blachere, J.M. Hettick, S. Lukomski, D. Schmechel, and D.H. Beezhold Characterization of recombinant terrelysin, a hemolysin of Aspergillus terreus Mycopathologia 171 2011 23 34
176. T. Tomita, K. Noguchi, H. Mimuro, F. Ukaji, K. Ito, N. Sugawara-Tomita, and Y. Hashimoto Pleurotolysin, a novel sphingomyelin-specific two-component cytolysin from the edible mushroom Pleurotus ostreatus, assembles into a transmembrane pore complex J. Biol. Chem. 279 2004 26975 26982
177. N. Sakurai, J. Kaneko, Y. Kamio, and T. Tomita Cloning, expression, and pore-forming properties of mature and precursor forms of pleurotolysin, a sphingomyelin-specific two-component cytolysin from the edible mushroom Pleurotus ostreatus Biochim. Biophys. Acta 1679 2004 65 73
178. S. Berne, K. Sepcic, G. Anderluh, T. Turk, P. Macek, and N. Poklar Ulrih Effect of pH on the pore forming activity and conformational stability of ostreolysin, a lipid raft-binding protein from the edible mushroom Pleurotus ostreatus Biochemistry 44 2005 11137 11147
179. K. Ota, A. Leonardi, M. Mikelj, M. Skocaj, T. Wohlschlager, M. Kunzler, M. Aebi, M. Narat, I. Krizaj, G. Anderluh, K. Sepcic, and P. Macek Membrane cholesterol and sphingomyelin, and ostreolysin A are obligatory for pore-formation by a MACPF/CDC-like pore-forming protein, pleurotolysin B Biochimie 95 2013 1855 1864
180. K. Sepcic, S. Berne, K. Rebolj, U. Batista, A. Plemenitas, M. Sentjurc, and P. Macek Ostreolysin, a pore-forming protein from the oyster mushroom, interacts specifically with membrane cholesterol-rich lipid domains FEBS Lett. 575 2004 81 85
181. K. Rebolj, N.P. Ulrih, P. Macek, and K. Sepcic Steroid structural requirements for interaction of ostreolysin, a lipid-raft binding cytolysin, with lipid monolayers and bilayers Biochim. Biophys. Acta 1758 2006 1662 1670
182. T. Shibata, M. Kudou, Y. Hoshi, A. Kudo, N. Nanashima, and K. Miyairi Isolation and characterization of a novel two-component hemolysin, erylysin A and B, from an edible mushroom, Pleurotus eryngii Toxicon 56 2010 1436 1442
183. H.B. Bhat, T. Kishimoto, M. Abe, A. Makino, T. Inaba, M. Murate, N. Dohmae, A. Kurahashi, K. Nishibori, F. Fujimori, P. Greimel, R. Ishitsuka, and T. Kobayashi Binding of a pleurotolysin ortholog from Pleurotus eryngii to sphingomyelin and cholesterol-rich membrane domains J. Lipid Res. 54 2013 2933 2943
184. H.H. Chowdhury, K. Rebolj, M. Kreft, R. Zorec, P. Macek, and K. Sepcic Lysophospholipids prevent binding of a cytolytic protein ostreolysin to cholesterol-enriched membrane domains Toxicon 51 2008 1345 1356
185. M. Skocaj, N. Resnik, M. Grundner, K. Ota, N. Rojko, V. Hodnik, G. Anderluh, A. Sobota, P. Macek, P. Veranic, and K. Sepcic Tracking cholesterol/sphingomyelin-rich membrane domains with the ostreolysin A-mCherry protein PLoS One 9 2014 e92783
186. Y. Sekizawa, T. Hagiwara, T. Nakajima, and H. Kobayashi A novel protein, lysenin, that causes contraction of the isolated rat aorta: its purification from the coelomic fluid of the earthworm, Eisenia foetida Biomed. Res. 17 1996 197 203
187. Y. Sekizawa, T. Kubo, H. Kobayashi, T. Nakajima, and S. Natori Molecular cloning of cDNA for lysenin, a novel protein in the earthworm Eisenia foetida that causes contraction of rat vascular smooth muscle Gene 191 1997 97 102
188. A. Yamaji-Hasegawa, A. Makino, T. Baba, Y. Senoh, H. Kimura-Suda, S.B. Sato, N. Terada, S. Ohno, E. Kiyokawa, M. Umeda, and T. Kobayashi Oligomerization and pore formation of a sphingomyelin-specific toxin, lysenin J. Biol. Chem. 278 2003 22762 22770
189. D. Fologea, E. Krueger, S. Rossland, S. Bryant, W. Foss, and T. Clark Cationic polymers inhibit the conductance of lysenin channels Sci. World J. 2013 2013 316758
190. R. Ishitsuka, and T. Kobayashi Cholesterol and lipid/protein ratio control the oligomerization of a sphingomyelin-specific toxin, lysenin Biochemistry 46 2007 1495 1502
191. A.B. Shakor, E.A. Czurylo, and A. Sobota Lysenin, a unique sphingomyelin-binding protein FEBS Lett. 542 2003 1 6
192. K. Hanada, K. Kumagai, S. Yasuda, Y. Miura, M. Kawano, M. Fukasawa, and M. Nishijima Molecular machinery for non-vesicular trafficking of ceramide Nature 426 2003 803 809
193. N. Sukumwang, and K. Umezawa Earthworm-derived pore-forming toxin lysenin and screening of its inhibitors Toxins (Basel) 5 2013 1392 1401
194. R.O. Brady, J.N. Kanfer, M.B. Mock, and D.S. Fredrickson The metabolism of sphingomyelin. II. Evidence of an enzymatic deficiency in Niemann-Pick disease Proc. Natl. Acad. Sci. U. S. A. 55 1966 366 369
195. T.V. Taksir, J. Johnson, C.L. Maloney, E. Yandl, D. Griffiths, B.L. Thurberg, and S. Ryan Optimization of a histopathological biomarker for sphingomyelin accumulation in acid sphingomyelinase deficiency J. Histochem. Cytochem. 60 2012 620 629
196. Y. Yoshida, K. Yoneda, M. Umeda, C. Ide, and K. Fujimoto Localization of sphingomyelin during the development of dorsal and tail epidermis of mice Br. J. Dermatol. 145 2001 758 770
197. T. Wang, H. Shogomori, M. Hara, T. Yamada, and T. Kobayashi Nanomechanical recognition of sphingomyelin-rich membrane domains by atomic force microscopy Biochemistry 51 2012 74 82
198. E.B. Neufeld, K. O'Brien, A.D. Walts, J.A. Stonik, D. Malide, C.A. Combs, and A.T. Remaley The human ABCG1 transporter mobilizes plasma membrane and late endosomal non-sphingomyelin-associated-cholesterol for efflux and esterification Biology 3 2014 866 891
199. J. Ikenouchi, M. Suzuki, K. Umeda, K. Ikeda, R. Taguchi, T. Kobayashi, S.B. Sato, T. Kobayashi, D.B. Stolz, and M. Umeda Lipid polarity is maintained in absence of tight junctions J. Biol. Chem. 287 2012 9525 9533
200. J. Ikenouchi, M. Hirata, S. Yonemura, and M. Umeda Sphingomyelin clustering is essential for the formation of microvilli J. Cell Sci. 126 2013 3585 3592
201. K. Kasahara, M. Kaneda, T. Miki, K. Iida, N. Sekino-Suzuki, I. Kawashima, H. Suzuki, M. Shimonaka, M. Arai, Y. Ohno-Iwashita, S. Kojima, M. Abe, T. Kobayashi, T. Okazaki, M. Souri, A. Ichinose, and N. Yamamoto Clot retraction is mediated by factor XIII-dependent fibrin-alphaIIbbeta3-myosin axis in platelet sphingomyelin-rich membrane rafts Blood 122 2013 3340 3348
202. Y. Kidani, K. Ohshima, H. Sakai, T. Kohno, A. Baba, and M. Hattori Differential localization of sphingomyelin synthase isoforms in neurons regulates sphingomyelin cluster formation Biochem. Biophys. Res. Commun. 417 2012 1014 1017
203. Y. Nagata, H. Kobayashi, M. Umeda, N. Ohta, S. Kawashima, P.S. Zammit, and R. Matsuda Sphingomyelin levels in the plasma membrane correlate with the activation state of muscle satellite cells J. Histochem. Cytochem. 54 2006 375 384
204. B. Brugger, B. Glass, P. Haberkant, I. Leibrecht, F.T. Wieland, and H.G. Krausslich The HIV lipidome: a raft with an unusual composition Proc. Natl. Acad. Sci. U. S. A. 103 2006 2641 2646
205. M. Lorizate, B. Brugger, H. Akiyama, B. Glass, B. Muller, G. Anderluh, F.T. Wieland, and H.G. Krausslich Probing HIV-1 membrane liquid order by Laurdan staining reveals producer cell-dependent differences J. Biol. Chem. 284 2009 22238 22247
206. R. Yachi, Y. Uchida, B.H. Balakrishna, G. Anderluh, T. Kobayashi, T. Taguchi, and H. Arai Subcellular localization of sphingomyelin revealed by two toxin-based probes in mammalian cells Genes Cells 17 2012 720 727