The C-terminal domain of perfringolysin O is an essential cholesterol-binding unit targeting to cholesterol-rich microdomains.

There is much evidence to indicate that cholesterol forms lateral membrane microdomains (rafts), and to suggest their important role in cellular signaling. However, no probe has been produced to analyze cholesterol behavior, especially cholesterol movement in rafts, in real time. To obtain a potent tool for analyzing cholesterol dynamics in rafts, we prepared and characterized several truncated fragments of theta-toxin (perfringolysin O), a cholesterol-binding cytolysin, whose chemically modified form has been recently shown to bind selectively to rafts. BIAcore and structural analyses demonstrate that the C-terminal domain (domain 4) of the toxin is the smallest functional unit that has the same cholesterol-binding activity as the full-size toxin with structural stability. Cell membrane-bound recombinant domain 4 was detected in the floating low-density fractions and was found to be cofractionated with the raft-associated protein Lck, indicating that recombinant domain 4 also binds selectively to cholesterol-rich rafts. Furthermore, an enhanced green fluorescent protein-domain 4 fusion protein stains membrane surfaces in a cholesterol-dependent manner in living cells. Therefore, domain 4 of theta-toxin is an essential cholesterol-binding unit targeting to cholesterol in membrane rafts, providing a very useful tool for further studies on lipid rafts on cell surfaces and inside cells.

[1]  M. Palmer,et al.  Streptolysin O: the C-terminal, tryptophan-rich domain carries functional sites for both membrane binding and self-interaction but not for stable oligomerization. , 2001, Biochimica et biophysica acta.

[2]  M. Umeda,et al.  Lysenin, a Novel Sphingomyelin-specific Binding Protein* , 1998, The Journal of Biological Chemistry.

[3]  A. Ostermeyer,et al.  Glycosphingolipids Are Not Essential for Formation of Detergent-resistant Membrane Rafts in Melanoma Cells , 1999, The Journal of Biological Chemistry.

[4]  J. Slot,et al.  Immunoelectron Microscopic Localization of Cholesterol Using Biotinylated and Non-cytolytic Perfringolysin O , 2002, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[5]  J. Slot,et al.  Selective binding of perfringolysin O derivative to cholesterol-rich membrane microdomains (rafts) , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[6]  H. Schägger,et al.  Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. , 1987, Analytical biochemistry.

[7]  N. Hooper Detergent-insoluble glycosphingolipid/cholesterol-rich membrane domains, lipid rafts and caveolae (review). , 1999, Molecular membrane biology.

[8]  Kai Simons,et al.  Lipid rafts and signal transduction , 2000, Nature Reviews Molecular Cell Biology.

[9]  R. Tweten,et al.  The mechanism of pore assembly for a cholesterol-dependent cytolysin: formation of a large prepore complex precedes the insertion of the transmembrane beta-hairpins. , 2000, Biochemistry.

[10]  T. Fujimoto,et al.  Crosslinked Plasmalemmal Cholesterol Is Sequestered to Caveolae: Analysis with a New Cytochemical Probe , 1997, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[11]  M. Nakamura,et al.  Contribution of tryptophan residues to the structural changes in perfringolysin O during interaction with liposomal membranes. , 1998, Journal of biochemistry.

[12]  A. Jonas,et al.  Surface plasmon resonance biosensor studies of human wild-type and mutant lecithin cholesterol acyltransferase interactions with lipoproteins. , 1999, Biochemistry.

[13]  L. Abrami,et al.  Landing on lipid rafts. , 1999, Trends in cell biology.

[14]  I. Morita,et al.  A biotinylated perfringolysin O derivative: a new probe for detection of cell surface cholesterol. , 1997, Biochimica et biophysica acta.

[15]  M. Nakamura,et al.  Contribution of individual tryptophan residues to the structure and activity of theta-toxin (perfringolysin O), a cholesterol-binding cytolysin. , 1996, European journal of biochemistry.

[16]  Michael W Parker,et al.  Structure of a Cholesterol-Binding, Thiol-Activated Cytolysin and a Model of Its Membrane Form , 1997, Cell.

[17]  J. Lakey,et al.  Brominated phospholipids as a tool for monitoring the membrane insertion of colicin A. , 1992, Biochemistry.

[18]  Tadashi Yamamoto,et al.  Association of Src Family Tyrosine Kinase Lyn with Ganglioside GD3 in Rat Brain , 1997, The Journal of Biological Chemistry.

[19]  H. Kawasaki,et al.  Cold-labile hemolysin produced by limited proteolysis of theta-toxin from Clostridium perfringens. , 1986, Biochemistry.

[20]  F. Studier,et al.  Use of T7 RNA polymerase to direct expression of cloned genes. , 1990, Methods in enzymology.

[21]  S. Iwashita,et al.  A modified theta-toxin produced by limited proteolysis and methylation: a probe for the functional study of membrane cholesterol. , 1990, Biochimica et biophysica acta.

[22]  P. W. Holloway,et al.  Quenching of tryptophan fluorescence by brominated phospholipid. , 1990, Biochemistry.

[23]  Y. Shimada,et al.  C-terminal Amino Acid Residues Are Required for the Folding and Cholesterol Binding Property of Perfringolysin O, a Pore-forming Cytolysin* , 1999, The Journal of Biological Chemistry.

[24]  E. Ikonen,et al.  Protein and lipid sorting from the trans-Golgi network to the plasma membrane in polarized cells. , 1998, Seminars in cell & developmental biology.

[25]  R. Parton,et al.  Ultrastructural localization of gangliosides; GM1 is concentrated in caveolae. , 1994, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[26]  U. K. Laemmli,et al.  Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4 , 1970, Nature.

[27]  M. Nakamura,et al.  Interaction of theta-toxin (perfringolysin O), a cholesterol-binding cytolysin, with liposomal membranes: change in the aromatic side chains upon binding and insertion. , 1995, Biochemistry.

[28]  S. Iwashita,et al.  Effect of lipidic factors on membrane cholesterol topology--mode of binding of theta-toxin to cholesterol in liposomes. , 1992, Biochimica et biophysica acta.

[29]  G. Moore,et al.  Rosette-forming human lymphoid cell lines. I. Establishment and evidence for origin of thymus-derived lymphocytes. , 1972, Journal of the National Cancer Institute.

[30]  S. Ando,et al.  Effect of isolated C-terminal fragment of theta-toxin (perfringolysin O) on toxin assembly and membrane lysis. , 1990, European journal of biochemistry.

[31]  Deborah A. Brown,et al.  Structure and Function of Sphingolipid- and Cholesterol-rich Membrane Rafts* , 2000, The Journal of Biological Chemistry.

[32]  F. Sanger,et al.  DNA sequencing with chain-terminating inhibitors. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[33]  J. Pitha,et al.  Intracellular Trafficking of Cholesterol Monitored with a Cyclodextrin* , 1996, The Journal of Biological Chemistry.

[34]  E. Ikonen,et al.  Functional rafts in cell membranes , 1997, Nature.

[35]  R. Tweten,et al.  Mechanism of membrane insertion of a multimeric beta-barrel protein: perfringolysin O creates a pore using ordered and coupled conformational changes. , 2000, Molecular cell.