Mega assemblages of oligomeric aerolysin-like toxins stabilized by toxin-associating membrane proteins

Journal of Biochemistry

Volumn 149, Issue 1, 2011, Pages 103-115

  Shimada, Hiroyasu ^a   Kitada, Sakae ^a  

^a KYUSHU INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

aerolysin; oligomer; parasporin; pore forming toxin

Indexed keywords

AEROLYSIN; ASSEMBLY 1; ASSEMBLY 2; CELL PROTEIN; CORE TOXIN COMPLEX; EPSILON TOXIN; GLYCOSIDASE; NUCLEASE; OLIGOMER; PARASPORIN 2; PROTEIN; PROTEINASE K; TOXIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; GEL PERMEATION CHROMATOGRAPHY; HUMAN; HUMAN CELL; NONHUMAN; PROTEIN DEGRADATION; TEMPERATURE DEPENDENCE;

ANIMALS; BACTERIAL TOXINS; CELL LINE; CELLS, CULTURED; DOGS; ENDOTOXINS; HUMANS; MEMBRANE PROTEINS; MOLECULAR WEIGHT; PORE FORMING CYTOTOXIC PROTEINS; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN MULTIMERIZATION; SODIUM DODECYL SULFATE;

EID: 78650648007     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvq124     Document Type: Article

References (60)

1. Gilbert, R.J. (2002) Inactivation and activity of cholesterol-dependent cytolysins: what structural studies tell us. Cell Mol. Life Sci. 59, 832-844
2. Parker, M.W. and Feil, S.C. (2005) Pore-forming protein toxins: from structure to function. Prog. Biophys. Mol. Biol. 88, 91-142
3. Heuck, A.P., Tweten, R.K., and Johnson, A.E. (2001) Beta-barrel pore-forming toxins: intriguing dimorphic proteins. Biochemistry 40, 9065-9073
4. Gonzalez, M.R., Bischofberger, M., Pernot, L., van der Goot, F.G., and Freche, B. (2008) Bacterial pore-forming toxins: the (w)hole story? Cell Mol. Life Sci. 65, 493-507
5. Iacovache, I., van der Goot, F.G., and Pernot, L. (2008) Pore formation: an ancient yet complex form of attack. Biochim. Biophys. Acta 1778, 1611-1623
6. Petit, L., Gibert, M., Gillet, D., Laurent-Winter, C, Boquet, P., and Popoff, M.R. (1997) Clostridium perfringens epsilon-toxin acts on MDCK cells by forming a large membrane complex. J. Bacteriol. 179, 6480-6487
7. van der Goot, F.G., Pattus, F., Parker, M., and Buckley, J.T. (1994) Toxicology 87, 19-28
8. Miller, C.J., Elliott, J.L., and Collier, R.J. (1999) Anthrax protective antigen: prepore-to-pore conversion. Biochemistry 38, 10432-10441
9. Hunter, S.E., Clarke, I.N., Kelly, D.C., and Titball, R.W. (1992) Cloning and nucleotide sequencing of the Clostridium perfringens epsilon-toxin gene and its expression in Escherichia coli. Infect. Immun. 60, 102-110
10. Tateno, H. and Goldstein, I.J. (2003) Molecular cloning, expression, and characterization of novel hemolytic lectins from the mushroom Laetiporus sulphureus, which show homology to bacterial toxins. J. Biol. Chem. 278, 40455-40463
11. Ito, A., Sasaguri, Y., Kitada, S., Kusaka, Y., Kuwano, K., Masutomi, K., Mizuki, E., Akao, T., and Ohba, M. (2004) A Bacillus thuringiensis crystal protein with selective cytocidal action to human cells. J. Biol. Chem. 279, 21282-21286
12. Howard, S.P. and Buckley, J.T. (1986) Molecular cloning and expression in Escherichia coli of the structural gene for the hemolytic toxin aerolysin from Aeromonas hydrophila. Mol. Gen. Genet. 204, 289-295
13. Parker, M.W., Buckley, J.T., Postma, J.P., Tucker, A.D., Leonard, K., Pattus, F., and Tsernoglou, D. (1994) Structure of the Aeromonas toxin proaerolysin in its water-soluble and membrane-channel states. Nature 367, 292-295
14. Cole, A.R., Gibert, M., Popoff, M., Moss, D.S., Titball, R.W., and Basak, A.K. (2004) Clostridium perfringens epsilon-toxin shows structural similarity to the pore-forming toxin aerolysin. Nat. Struct. Mol. Biol. 11, 797-798
15. Akiba, T., Abe, Y., Kitada, S., Kusaka, Y., Ito, A., Ichimatsu, T., Katayama, H., Akao, T., Higuchi, K, Mizuki, E., Ohba, M., Kanai, R., and Harata, K. (2009) Crystal Structure of the Parasporin-2 Bacillus thuringiensis Toxin That Recognizes Cancer Cells. J. Mol. Biol. 386, 121-133
16. Payne, D.W., Williamson, E.D., Havard, H., Modi, N., and Brown, J. (1994) Evaluation of a new cytotoxicity assay for Clostridium perfringens type D epsilon toxin. FEMS Microbiol. Lett. 116, 161-167 (Pubitemid 124011993)
17. Kitada, S., Abe, Y., Shimada, H., Kusaka, Y., Matsuo, Y., Katayama, H., Okumura, S., Akao, T., Mizuki, E., Kuge, O., Sasaguri, Y., Ohba, M., and Ito, A. (2006) Cytocidal actions of parasporin-2, an anti-tumor crystal toxin from Bacillus thuringiensis. J. Biol. Chem. 281, 26350-26360
18. Katayama, H., Yokota, H., Akao, T., Nakamura, O., Ohba, M., Mekada, E., and Mizuki, E. (2005) Parasporin-1, a novel cytotoxic protein to human cells from non-insecticidal parasporal inclusions of Bacillus thuringiensis. J. Biochem. 137, 17-25
19. Saitoh, H., Okumura, S., Ishikawa, T., Akao, T., Mizuki, E., and Ohba, M. (2006) Investigation of a novel Bacillus thuringiensis gene encoding a parasporal protein, parasporin-4, that preferentially kills human leukemic T cells. Biosci. Biotechnol. Biochem. 70, 2935-2941
20. Yamashita, S., Katayama, H, Saitoh, H, Akao, T., Park, Y.S., Mizuki, E., Ohba, M., and Ito, A. (2005) Typical three-domain cry proteins of Bacillus thuringiensis strain A1462 exhibit cytocidal activity on limited human cancer cells. J. Biochem. 138, 663-672
21. Ohba, M., Mizuki, E., and Uemori, A. (2009) Parasporin, a new anticancer protein group from Bacillus thuringiensis. Anticancer Res. 29, 427-433
22. Abe, Y., Shimada, H., and Kitada, S. (2008) Raft-targeting and Oligomerization of Parasporin-2, a Bacillus thuringiensis Crystal Protein with Anti-Tumour Activity. J. Biochem. 143, 269-275
23. Kitada, S., Abe, Y., Maeda, T., and Shimada, H. (2009) Parasporin-2 requires GPI-anchored proteins for the efficient cytocidal action to human hepatoma cells. Toxicology 264, 80-88
24. Bhakdi, S. and Tranum-Jensen, J. (1991) Alpha-toxin of Staphylococcus aureus. Microbiol. Rev. 55, 733-751
25. Alouf, J.E. (2000) Cholesterol-binding cytolytic protein toxins. Int. J. Med. Microbiol. 290, 351-356
26. Walsh, D.M., Klyubin, I., Fadeeva, J.V., Cullen, W.K., Anwyl, R., Wolfe, M.S., Rowan, M.J., and Selkoe, D.J. (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416, 535-539
27. Sindi, S.S. and Serio, T.R. (2009) Prion dynamics and the quest for the genetic determinant in protein-only inheritance. Curr. Opin. Microbiol. 12, 623-630
28. Scherzinger, E., Lurz, R., Turmaine, M., Mangiarini, L., Hollenbach, B., Hasenbank, R., Bates, G.P., Davies, S.W., Lehrach, H., and Wanker, E.E. (1997) Huntingtin-encoded polyglutamine expansions form amyloid-like protein aggregates in vitro and in vivo. Cell 90, 549-558
29. Fink, A.L. (2006) The aggregation and fibrillation of alpha-synuclein. Acc. Chem. Res. 39, 628-634
30. Zheng, J., Jang, H, Ma, B., Tsai, C.J., and Nussinov, R. (2007) Modeling the Alzheimer Abeta17-42 fibril architecture: tight intermolecular sheet-sheet association and intramolecular hydrated cavities. Biophys. J. 93, 3046-3057
31. Collinge, J. (2001) Prion diseases of humans and animals: their causes and molecular basis. Annu. Rev. Neurosci. 24, 519-550
32. Pan, K.M., Baldwin, M., Nguyen, J., Gasset, M., Serban, A., Groth, D., Mehlhorn, I., Huang, Z., Fletterick, R.J., Cohen, F.E., and Prusiner, S.B. (1993) Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins. Proc. Natl Acad. Sci. USA 90, 10962-10966
33. Serpell, L.C. (2000) Alzheimer's amyloid fibrils: structure and assembly. Biochim. Biophys. Acta 1502, 16-30
34. DiFiglia, M., Sapp, E., Chase, K.O., Davies, S.W., Bates, G.P., Vonsattel, J.P., and Aronin, N. (1997) Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 277, 1990-1993
35. MacDonald, M.E., Ambrose, CM., Duyao, M.P., Myers, R.H., Lin, C, Srinidhi, L., Barnes, G., Taylor, S.A., James, M., Groot, N, MacFarlane, H., Jenkins, B., Anderson, M.A., Wexler, N.S., Gusella, J.F., Bates, G.P., Baxendale, S., Hummerich, H., Kirby, S., North, M., Youngman, S., Mott, R., Zehetner, G., Sedlacek, Z., Poustka, A., Frischauf, A.-M., Lehrach, H., Buckler, A.J., Church, D., Doucette-Stamm, L., O'Donovan, M.C., Riba-Ramirez, L., Shah, M., Stanton, V.P., Strobel, S.A., Draths, K.M., Wales, J.L., Dervan, P., Housman, D.E., Altherr, M., Shiang, R., Thompson, L., Fielder, T., Wasmuth, J.J., Tagle, D., Valdes, J., Elmer, L., Allard, M., Castilla, L., Swaroop, M., Blanchard, K, Collins, F.S., Snell, R., Holloway, T., Gillespie, K, Datson, N, Shaw, D., and Harper, P.S. (1993) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 72, 971-983
36. Gutekunst, C.A., Li, S.H., Yi, H., Mulroy, J.S., Kuemmerle, S., Jones, R., Rye, D., Ferrante, R. J., Hersch, S.M., and Li, X.J. (1999) Nuclear and neuropil aggregates in Huntington's disease: relationship to neuropathology. J. Neurosci. 19, 2522-2534
37. Abrami, L. and van Der Goot, F.G. (1999) Plasma membrane microdomains act as concentration platforms to facilitate intoxication by aerolysin. J. Cell Biol 147, 175-184
38. van der Goot, F.G., Pattus, F., Wong, K.R., and Buckley, J.T. (1993) Oligomerization of the channel-forming toxin aerolysin precedes insertion into lipid bilayers. Biochemistry 32, 2636-2642
39. Nagahama, M., Hara, H., Fernandez-Miyakawa, M., Itohayashi, Y., and Sakurai, J. (2006) Oligomerization of Clostridium perfringens epsilon-toxin is dependent upon membrane fluidity in liposomes. Biochemistry 45, 296-302
40. Bietlot, H.P., Schernthaner, J.P., Milne, R.E., Clairmont, F.R., Bhella, R.S., and Kaplan, H. (1993) Evidence that the CryIA crystal protein from Bacillus thuringiensis is associated with DNA. J. Biol. Chem. 268, 8240-8245
41. Xia, L., Sun, Y., Ding, X., Fu, Z., Mo, X., Zhang, H., and Yuan, Z. (2005) Identification of cry-type genes on 20-kb DNA associated with Cry1 crystal proteins from Bacillus thuringiensis. Curr. Microbiol. 51, 53-58
42. Abrami, L., Velluz, M.C., Hong, Y., Ohishi, K., Mehlert, A., Ferguson, M., Kinoshita, T., and Gisou van der Goot, F. (2002) The glycan core of GPI-anchored proteins modulates aerolysin binding but is not sufficient: The polypeptide moiety is required for the toxin-receptor interaction. FEBS Lett. 512, 249-254
43. Shimamoto, S., Tamai, E., Matsushita, O., Minami, J., Okabe, A., and Miyata, S. (2005) Changes in ganglioside content affect the binding of Clostridium perfringens epsilon-toxin to detergent-resistant membranes of Madin-Darby canine kidney cells. Microbiol. Immunol. 49, 245-253
44. Tsitrin, Y., Morton, C.J., el-Bez, C, Paumard, P., Velluz, M.C., Adrian, M., Dubochet, J., Parker, M.W., Lanzavecchia, S., and van der Goot, F.G. (2002) Conversion of a transmembrane to a water-soluble protein complex by a single point mutation. Nat. Struct. Biol. 9, 729-733
45. Diep, D.B., Nelson, K.L., Raja, S.M., Pleshak, E.N., and Buckley, J.T. (1998) Glycosylphosphatidylinositol anchors of membrane glycoproteins are binding determinants for the channel-forming toxin aerolysin. J. Biol. Chem. 273, 2355-2360
46. Abrami, L., Fivaz, M., Glauser, P.E., Parton, R.G., and van der Goot, F.G. (1998) A pore-forming toxin interacts with a GPI-anchored protein and causes vacuolation of the endoplasmic reticulum. J. Cell Biol 140, 525-540
47. Miyata, S., Minami, J., Tamai, E., Matsushita, O., Shimamoto, S., and Okabe, A. (2002) Clostridium perfringens epsilon-toxin forms a heptameric pore within the detergent-insoluble microdomains of Madin-Darby canine kidney cells and rat synaptosomes. J. Biol. Chem. 277, 39463-39468
48. 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
49. Tweten, R.K. (2005) Cholesterol-dependent cytolysins, a family of versatile pore-forming toxins. Infect. Immun. 73, 6199-6209
50. Palmer, M. (2001) The family of thiol-activated, cholesterol-binding cytolysins. Toxicon 39, 1681-1689
51. Gilbert, R.J. (2005) Inactivation and activity of cholesterol-dependent cytolysins: what structural studies tell us. Structure 13, 1097-1106
52. Tilley, S.J., Orlova, E.V., Gilbert, R.J., Andrew, P.W., and Saibil, H.R. (2005) tructural basis of pore formation by the bacterial toxin pneumolysin. Cell 121, 247-256
53. Czajkowsky, D.M., Hotze, E.M., Shao, Z., and Tweten, R.K. (2004) Vertical collapse of a cytolysin prepore moves its transmembrane beta-hairpins to the membrane. EMBO J. 23, 3206-3215
54. Olofsson, A., Hebert, H., and Thelestam, M. (1993) The projection structure of perfringolysin O (Clostridium perfringens theta-toxin). FEBS Lett. 319, 125-127
55. Petit, L., Maier, E., Gibert, M., Popoff, M.R., and Benz, R. (2001) J. Biol. Chem. 276, 15736-15740
56. Lashuel, H.A., Hartley, D., Petre, B.M., Walz, T., and Lansbury, P.T. Jr (2002) Neurodegenerative disease: amyloid pores from pathogenic mutations. Nature 418, 291
57. Demuro, A., Mina, E., Kayed, R., Milton, S.C., Parker, I., and Glabe, C.G. (2005) Calcium dysregulation and membrane disruption as a ubiquitous neurotoxic mechanism of soluble amyloid oligomers. J. Biol. Chem. 280, 17294-17300
58. Kayed, R., Head, E., Thompson, J.L., McIntire, T.M., Milton, S.C., Cotman, C.W., and Glabe, C.G. (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486-489
59. Kayed, R., Sokolov, Y., Edmonds, B., McIntire, T.M., Milton, S.C., Hall, J.E., and Glabe, C.G. (2004) Permeabilization of lipid bilayers is a common conformation-dependent activity of soluble amyloid oligomers in protein misfolding diseases. J. Biol. Chem. 279, 46363-46366
60. Nijtmans, L.G., Henderson, N.S., and Holt, I.J. (2002) Blue Native electrophoresis to study mitochondrial and other protein complexes. Methods 26, 327-334