1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Microbiology
  4. Volume 69, 2015
  5. Article

Annual Review of Microbiology

Volume 69, 2015

The Unique Molecular Choreography of Giant Pore Formation by the Cholesterol-Dependent Cytolysins of Gram-Positive Bacteria

Abstract

The mechanism by which the cholesterol-dependent cytolysins (CDCs) assemble their giant β-barrel pore in cholesterol-rich membranes has been the subject of intense study in the past two decades. A combination of structural, biophysical, and biochemical analyses has revealed deep insights into the series of complex and highly choreographed secondary and tertiary structural transitions that the CDCs undergo to assemble their β-barrel pore in eukaryotic membranes. Our knowledge of the molecular details of these dramatic structural changes in CDCs has transformed our understanding of how giant pore complexes are assembled and has been critical to our understanding of the mechanisms of other important classes of pore-forming toxins and proteins across the kingdoms of life. Finally, there are tantalizing hints that the CDC pore-forming mechanism is more sophisticated than previously imagined and that some CDCs are employed in pore-independent processes.

Keyword(s): CD59, intermedilysin, perfringolysin O, sterol, streptolysin O, β-barrel
Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-091014-104233
2015-10-15
2024-04-30
Loading full text...

Full text loading...

/deliver/fulltext/micro/69/1/annurev-micro-091014-104233.html?itemId=/content/journals/10.1146/annurev-micro-091014-104233&mimeType=html&fmt=ahah

Literature Cited

  1. Balachandran P, Hollingshead SK, Paton JC, Briles DE. 1.  2001. The autolytic enzyme LytA of Streptococcus pneumoniae is not responsible for releasing pneumolysin. J. Bacteriol. 183:3108–16 [Google Scholar]
  2. Benton KA, Everson MP, Briles DE. 2.  1995. A pneumolysin-negative mutant of Streptococcus pneumoniae causes chronic bacteremia rather than acute sepsis in mice. Infect. Immun. 63:448–55 [Google Scholar]
  3. Benton KA, Paton JC, Briles DE. 3.  1997. Differences in virulence for mice among Streptococcus pneumoniae strains of capsular types 2, 3, 4, 5, and 6 are not attributable to differences in pneumolysin production. Infect. Immun. 65:1237–44 [Google Scholar]
  4. Bourdeau RW, Malito E, Chenal A, Bishop BL, Musch MW. 4.  et al. 2009. Cellular functions and X-ray structure of anthrolysin O, a cholesterol-dependent cytolysin secreted by Bacillus anthracis. J. Biol. Chem. 284:14645–56 [Google Scholar]
  5. Bricker AL, Carey VJ, Wessels MR. 5.  2005. Role of NADase in virulence in experimental invasive group A streptococcal infection. Infect. Immun. 73:6562–66 [Google Scholar]
  6. Bricker AL, Cywes C, Ashbaugh CD, Wessels MR. 6.  2002. NAD+-glycohydrolase acts as an intracellular toxin to enhance the extracellular survival of group A streptococci. Mol. Microbiol. 44:257–69 [Google Scholar]
  7. Cohen B, Shwachman H, Perkins ME. 7.  1937. Inactivation of pneumococcal hemolysin by certain sterols. Exp. Biol. Med. 35:586–91 [Google Scholar]
  8. Czajkowsky DM, Hotze EM, Shao Z, Tweten RK. 8.  2004. Vertical collapse of a cytolysin prepore moves its transmembrane β-hairpins to the membrane. EMBO J. 23:3206–15 [Google Scholar]
  9. Dowd KJ, Farrand AJ, Tweten RK. 9.  2012. The cholesterol-dependent cytolysin signature motif: a critical element in the allosteric pathway that couples membrane binding to pore assembly. PLOS Pathog. 8:e1002787 [Google Scholar]
  10. Dunstone MA, Tweten RK. 10.  2012. Packing a punch: the mechanism of pore formation by cholesterol dependent cytolysins and membrane attack complex/perforin-like proteins. Curr. Opin. Struct. Biol. 22:342–49 [Google Scholar]
  11. Ehrlich P. 11.  1898. Diskussionsbemerkungen (Crotin und Tetanolysin). Berlin Klin. Wochenschr. 36:273–74 [Google Scholar]
  12. Fang Y, Cheley S, Bayley H, Yang J. 12.  1997. The heptameric prepore of a staphylococcal alpha-hemolysin mutant in lipid bilayers imaged by atomic force microscopy. Biochemistry 36:9518–22 [Google Scholar]
  13. Farrand AJ, Hotze EM, Sato TK, Wade KR, Wimley WC. 13.  et al. 2015. The cholesterol-dependent cytolysin membrane-binding interface discriminates lipid environments of cholesterol to support β-barrel pore insertion. J. Biol. Chem. 29017733–44
  14. Farrand AJ, LaChapelle S, Hotze EM, Johnson AE, Tweten RK. 14.  2010. Only two amino acids are essential for cytolytic toxin recognition of cholesterol at the membrane surface. PNAS 107:4341–46 [Google Scholar]
  15. Feil SC, Ascher DB, Kuiper MJ, Tweten RK, Parker MW. 15.  2014. Structural studies of Streptococcus pyogenes streptolysin O provide insights into the early steps of membrane penetration. J. Mol. Biol. 426:785–92 [Google Scholar]
  16. Flanagan JJ, Tweten RK, Johnson AE, Heuck AP. 16.  2009. Cholesterol exposure at the membrane surface is necessary and sufficient to trigger perfringolysin O binding. Biochemistry 48:3977–87 [Google Scholar]
  17. Garland WJ, Buckley JT. 17.  1988. The cytolytic toxin aerolysin must aggregate to disrupt erythrocytes, and aggregation is stimulated by human glycophorin. Infect. Immun. 56:1249–53 [Google Scholar]
  18. Gelber SE, Aguilar JL, Lewis KL, Ratner AJ. 18.  2008. Functional and phylogenetic characterization of Vaginolysin, the human-specific cytolysin from Gardnerella vaginalis. J. Bacteriol. 190:3896–903 [Google Scholar]
  19. Giddings KS, Johnson AE, Tweten RK. 19.  2003. Redefining cholesterol's role in the mechanism of the cholesterol-dependent cytolysins. PNAS 100:11315–20 [Google Scholar]
  20. Giddings KS, Zhao J, Sims PJ, Tweten RK. 20.  2004. Human CD59 is a receptor for the cholesterol-dependent cytolysin intermedilysin. Nat. Struct. Mol. Biol. 11:1173–78 [Google Scholar]
  21. Hadders MA, Beringer DX, Gros P. 21.  2007. Structure of C8α-MACPF reveals mechanism of membrane attack in complement immune defense. Science 317:1552–54 [Google Scholar]
  22. Hamon MA, Ribet D, Stavru F, Cossart P. 22.  2012. Listeriolysin O: the Swiss army knife of Listeria. Trends Microbiol. 20:360–68 [Google Scholar]
  23. Heuck AP, Hotze E, Tweten RK, Johnson AE. 23.  2000. Mechanism of membrane insertion of a multimeric β-barrel protein: Perfringolysin O creates a pore using ordered and coupled conformational changes. Mol. Cell 6:1233–42 [Google Scholar]
  24. Heuck AP, Tweten RK, Johnson AE. 24.  2003. Assembly and topography of the prepore complex in cholesterol-dependent cytolysins. J. Biol. Chem. 278:31218–25 [Google Scholar]
  25. Hotze EM, Heuck AP, Czajkowsky DM, Shao Z, Johnson AE, Tweten RK. 25.  2002. Monomer-monomer interactions drive the prepore to pore conversion of a β-barrel-forming cholesterol-dependent cytolysin. J. Biol. Chem. 277:11597–605 [Google Scholar]
  26. Hotze EM, Le HM, Sieber JR, Bruxvoort C, McInerney MJ, Tweten RK. 26.  2013. Identification and characterization of the first cholesterol-dependent cytolysins from gram-negative bacteria. Infect. Immun. 81:216–25 [Google Scholar]
  27. Hotze EM, Wilson-Kubalek E, Farrand AJ, Bentsen L, Parker MW. 27.  et al. 2012. Monomer-monomer interactions propagate structural transitions necessary for pore formation by the cholesterol-dependent cytolysins. J. Biol. Chem. 287:24534–43 [Google Scholar]
  28. Hotze EM, Wilson-Kubalek EM, Rossjohn J, Parker MW, Johnson AE, Tweten RK. 28.  2001. Arresting pore formation of a cholesterol-dependent cytolysin by disulfide trapping synchronizes the insertion of the transmembrane beta-sheet from a prepore intermediate. J. Biol. Chem. 276:8261–68 [Google Scholar]
  29. Howard JG, Wallace KR, Wright GP. 29.  1953. The inhibitory effects of cholesterol and related sterols on haemolysis by streptolysin O. Br. J. Exp. Pathol. 34:174–80 [Google Scholar]
  30. Huang Y, Qiao F, Abagyan R, Hazard S, Tomlinson S. 30.  2006. Defining the CD59-C9 binding interaction. J. Biol. Chem. 281:27398–404 [Google Scholar]
  31. Iwamoto M, Ohno-Iwashita Y, Ando S. 31.  1987. Role of the essential thiol group in the thiol-activated cytolysin from Clostridium perfringens. Eur. J. Biochem. 167:425–30 [Google Scholar]
  32. Johnson BB, Moe PC, Wang D, Rossi K, Trigatti BL, Heuck AP. 32.  2012. Modifications in perfringolysin O domain 4 alter the cholesterol concentration threshold required for binding. Biochemistry 51:3373–82 [Google Scholar]
  33. Johnson MK. 33.  1977. Cellular location of pneumolysin. FEMS Microbiol. Lett. 2:243–45 [Google Scholar]
  34. Johnson S, Brooks NJ, Smith RA, Lea SM, Bubeck D. 34.  2013. Structural basis for recognition of the pore-forming toxin intermedilysin by human complement receptor CD59. Cell Rep. 3:1369–77 [Google Scholar]
  35. Jost BH, Lucas EA, Billington SJ, Ratner AJ, McGee DJ. 35.  2011. Arcanolysin is a cholesterol-dependent cytolysin of the human pathogen Arcanobacterium haemolyticum. BMC Microbiol. 11:239 [Google Scholar]
  36. Kacprzyk-Stokowiec A, Kulma M, Traczyk G, Kwiatkowska K, Sobota A, Dadlez M. 36.  2014. Crucial role of perfringolysin O D1 domain in orchestrating structural transitions leading to membrane-perforating pores: a hydrogen-deuterium exchange study. J. Biol. Chem. 289:28738–52 [Google Scholar]
  37. Kawate T, Gouaux E. 37.  2003. Arresting and releasing Staphylococcal α-hemolysin at intermediate stages of pore formation by engineered disulfide bonds. Protein Sci. 12:997–1006 [Google Scholar]
  38. Kehoe MA, Miller L, Walker JA, Boulnois GJ. 38.  1987. Nucleotide sequence of the streptolysin O (SLO) gene: structural homologies between SLO and other membrane-damaging, thiol-activated toxins. Infect. Immun. 55:3228–32 [Google Scholar]
  39. Koster S, van Pee K, Hudel M, Leustik M, Rhinow D. 39.  et al. 2014. Crystal structure of listeriolysin O reveals molecular details of oligomerization and pore formation. Nat. Commun. 5:3690 [Google Scholar]
  40. LaChapelle S, Tweten RK, Hotze EM. 40.  2009. Intermedilysin-receptor interactions during assembly of the pore complex: assembly intermediates increase host cell susceptibility to complement-mediated lysis. J. Biol. Chem. 284:12719–26 [Google Scholar]
  41. Law RH, Lukoyanova N, Voskoboinik I, Caradoc-Davies TT, Baran K. 41.  et al. 2010. The structural basis for membrane binding and pore formation by lymphocyte perforin. Nature 468:447–51 [Google Scholar]
  42. Leung C, Dudkina NV, Lukoyanova N, Hodel AW, Farabella I. 42.  et al. 2014. Stepwise visualization of membrane pore formation by suilysin, a bacterial cholesterol-dependent cytolysin. eLife 3:e04247 [Google Scholar]
  43. Los FC, Randis TM, Aroian RV, Ratner AJ. 43.  2013. Role of pore-forming toxins in bacterial infectious diseases. Microbiol. Mol. Biol. Rev. 77:173–207 [Google Scholar]
  44. Lukoyanova N, Kondos SC, Farabella I, Law RHP, Reboul CF. 44.  et al. 2015. Conformational changes during pore formation by the perforin-related protein pleurotolysin. PLOS Biol. 13:2e1002049 [Google Scholar]
  45. Madden JC, Ruiz N, Caparon M. 45.  2001. Cytolysin-mediated translocation (CMT): a functional equivalent of type III secretion in gram-positive bacteria. Cell 104:143–52 [Google Scholar]
  46. Magassa N, Chandrasekaran S, Caparon MG. 46.  2010. Streptococcus pyogenes cytolysin-mediated translocation does not require pore formation by streptolysin O. EMBO Rep. 5:400–5 [Google Scholar]
  47. Marchioretto M, Podobnik M, Dalla Serra M, Anderluh G. 47.  2013. What planar lipid membranes tell us about the pore-forming activity of cholesterol-dependent cytolysins. Biophys. Chem. 182:64–70 [Google Scholar]
  48. Marriott HM, Mitchell TJ, Dockrell DH. 48.  2008. Pneumolysin: a double-edged sword during the host-pathogen interaction. Curr. Mol. Med. 8:497–509 [Google Scholar]
  49. Meehl MA, Caparon MG. 49.  2004. Specificity of streptolysin O in cytolysin-mediated translocation. Mol. Microbiol. 52:1665–76 [Google Scholar]
  50. Melton-Witt JA, Bentsen LM, Tweten RK. 50.  2006. Identification of functional domains of Clostridium septicum alpha toxin. Biochemistry 45:14347–54 [Google Scholar]
  51. Mengaud J, Vicente MF, Chenevert J, Pereira JM, Geoffroy C. 51.  et al. 1988. Expression in Escherichia coli and sequence analysis of the listeriolysin O determinant of Listeria monocytogenes. Infect. Immun. 56:766–72 [Google Scholar]
  52. Miller CJ, Elliot JL, Collier RL. 52.  1999. Anthrax protective antigen: prepore-to-pore conversion. Biochemistry 38:10432–41 [Google Scholar]
  53. Mozola CC, Magassa N, Caparon MG. 53.  2014. A novel cholesterol-insensitive mode of membrane binding promotes cytolysin-mediated translocation by streptolysin O. Mol. Microbiol. 94:675–87 [Google Scholar]
  54. Murzin AG, Lesk AM, Chothia C. 54.  1994. Principles determining the structure of β-sheet barrels in proteins. I. A theoretical analysis. J. Mol. Biol. 236:1369–81 [Google Scholar]
  55. Murzin AG, Lesk AM, Chothia C. 55.  1994. Principles determining the structure of β-sheet barrels in proteins. II. The observed structures. J. Mol. Biol. 236:1382–400 [Google Scholar]
  56. Nagamune H, Ohnishi C, Katsuura A, Fushitani K, Whiley RA. 56.  et al. 1996. Intermedilysin, a novel cytotoxin specific for human cells secreted by Streptococcus intermedius UNS46 isolated from a human liver abscess. Infect. Immun. 64:3093–100 [Google Scholar]
  57. Nakamura M, Sekino N, Iwamoto M, Ohno-Iwashita Y. 57.  1995. Interaction of θ-toxin (perfringolysin O), a cholesterol-binding cytolysin, with liposomal membranes: change in the aromatic side chains upon binding and insertion. Biochemistry 34:6513–20 [Google Scholar]
  58. Nakano Y, Noda K, Endo T, Kobata A, Tomita M. 58.  1994. Structural study on the glycosyl-phosphatidylinositol anchor and the asparagine-linked sugar chain of a soluble form of CD59 in human urine. Arch. Biochem. Biophys. 311:117–26 [Google Scholar]
  59. Nelson LD, Chiantia S, London E. 59.  2010. Perfringolysin O association with ordered lipid domains: implications for transmembrane protein raft affinity. Biophys. J. 99:3255–63 [Google Scholar]
  60. Nelson LD, Johnson AE, London E. 60.  2008. How interaction of perfringolysin O with membranes is controlled by sterol structure, lipid structure, and physiological low pH: insights into the origin of perfringolysin O-lipid raft interaction. J. Biol. Chem. 283:4632–42 [Google Scholar]
  61. O'Seaghdha M, Wessels MR. 61.  2013. Streptolysin O and its co-toxin NAD-glycohydrolase protect group A Streptococcus from xenophagic killing. PLOS Pathog. 9:e1003394 [Google Scholar]
  62. Palmer M, Vulicevic I, Saweljew P, Valeva A, Kehoe M, Bhakdi S. 62.  1998. Streptolysin O: a proposed model of allosteric interaction between a pore-forming protein and its target lipid bilayer. Biochemistry 37:2378–83 [Google Scholar]
  63. Panchal RG, Bayley H. 63.  1995. Interactions between residues in staphylococcal α-hemolysin revealed by reversion mutagenesis. J. Biol. Chem. 270:23072–76 [Google Scholar]
  64. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM. 64.  et al. 2004. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25:1605–12 [Google Scholar]
  65. Polekhina G, Giddings KS, Tweten RK, Parker MW. 65.  2005. Insights into the action of the superfamily of cholesterol-dependent cytolysins from studies of intermedilysin. PNAS 102:600–5 [Google Scholar]
  66. Price KE, Camilli A. 66.  2009. Pneumolysin localizes to the cell wall of Streptococcus pneumoniae. J. Bacteriol. 191:2163–68 [Google Scholar]
  67. Price KE, Greene NG, Camilli A. 67.  2012. Export requirements of pneumolysin in Streptococcus pneumoniae. J. Bacteriol. 194:3651–60 [Google Scholar]
  68. Prigent D, Alouf JE. 68.  1976. Interaction of streptolysin-O with sterols. Biochim. Biophys. Acta 443:288–300 [Google Scholar]
  69. Ramachandran R, Heuck AP, Tweten RK, Johnson AE. 69.  2002. Structural insights into the membrane-anchoring mechanism of a cholesterol-dependent cytolysin. Nat. Struct. Biol. 9:823–27 [Google Scholar]
  70. Ramachandran R, Tweten RK, Johnson AE. 70.  2004. Membrane-dependent conformational changes initiate cholesterol-dependent cytolysin oligomerization and intersubunit β-strand alignment. Nat. Struct. Mol. Biol. 11:697–705 [Google Scholar]
  71. Ramachandran R, Tweten RK, Johnson AE. 71.  2005. The domains of a cholesterol-dependent cytolysin undergo a major FRET-detected rearrangement during pore formation. PNAS 102:7139–44 [Google Scholar]
  72. Reboul CF, Mahmood K, Whisstock JC, Dunstone MA. 72.  2012. Predicting giant transmembrane β-barrel architecture. Bioinformatics 28:1299–302 [Google Scholar]
  73. Reboul CF, Whisstock JC, Dunstone MA. 73.  2014. A new model for pore formation by cholesterol-dependent cytolysins. PLOS Comput. Biol. 10:e1003791 [Google Scholar]
  74. Robertson SL, Li J, Uzal FA, McClane BA. 74.  2011. Evidence for a prepore stage in the action of Clostridium perfringens epsilon toxin. PLOS ONE 6:e22053 [Google Scholar]
  75. Rollins SA, Sims PJ. 75.  1990. The complement-inhibitory activity of CD59 resides in its capacity to block incorporation of C9 into membrane C5b-9. J. Immunol. 144:3478–83 [Google Scholar]
  76. Rosado CJ, Buckle AM, Law RH, Butcher RE, Kan WT. 76.  et al. 2007. A common fold mediates vertebrate defense and bacterial attack. Science 317:1548–51 [Google Scholar]
  77. Rosado CJ, Kondos S, Bull TE, Kuiper MJ, Law RH. 77.  et al. 2008. The MACPF/CDC family of pore-forming toxins. Cell. Microbiol. 10:1765–74 [Google Scholar]
  78. Rossjohn J, Feil SC, McKinstry WJ, Tweten RK, Parker MW. 78.  1997. Structure of a cholesterol-binding thiol-activated cytolysin and a model of its membrane form. Cell 89:685–92 [Google Scholar]
  79. Rossjohn J, Polekhina G, Feil SC, Morton CJ, Tweten RK, Parker MW. 79.  2007. Structures of perfringolysin O suggest a pathway for activation of cholesterol-dependent cytolysins. J. Mol. Biol. 367:1227–36 [Google Scholar]
  80. Sato TK, Tweten RK, Johnson AE. 80.  2013. Disulfide-bond scanning reveals assembly state and β-strand tilt angle of the PFO β-barrel. Nat. Chem. Biol. 9:383–89 [Google Scholar]
  81. Sekino-Suzuki N, Nakamura M, Mitsui KI, Ohno-Iwashita Y. 81.  1996. Contribution of individual tryptophan residues to the structure and activity of θ-toxin (perfringolysin O), a cholesterol-binding cytolysin. Eur. J. Biochem. 241:941–47 [Google Scholar]
  82. Sellman BR, Kagan BL, Tweten RK. 82.  1997. Generation of a membrane-bound, oligomerized pre-pore complex is necessary for pore formation by Clostridium septicum alpha toxin. Mol. Microbiol. 23:551–58 [Google Scholar]
  83. Seveau S. 83.  2014. Multifaceted activity of listeriolysin O, the cholesterol-dependent cytolysin of Listeria monocytogenes. Subcell. Biochem. 80:161–95 [Google Scholar]
  84. Shatursky O, Heuck AP, Shepard LA, Rossjohn J, Parker MW. 84.  et al. 1999. The mechanism of membrane insertion for a cholesterol dependent cytolysin: a novel paradigm for pore-forming toxins. Cell 99:293–99 [Google Scholar]
  85. Shepard LA, Heuck AP, Hamman BD, Rossjohn J, Parker MW. 85.  et al. 1998. Identification of a membrane-spanning domain of the thiol-activated pore-forming toxin Clostridium perfringens perfringolysin O: an α-helical to β-sheet transition identified by fluorescence spectroscopy. Biochemistry 37:14563–74 [Google Scholar]
  86. Shepard LA, Shatursky O, Johnson AE, Tweten RK. 86.  2000. The mechanism of assembly and insertion of the membrane complex of the cholesterol-dependent cytolysin perfringolysin O: Formation of a large prepore complex. Biochemistry 39:10284–93 [Google Scholar]
  87. Shewell LK, Harvey RM, Higgins MA, Day CJ, Hartley-Tassell LE. 87.  et al. 2014. The cholesterol-dependent cytolysins pneumolysin and streptolysin O require binding to red blood cell glycans for hemolytic activity. PNAS 111:49E5312–20 [Google Scholar]
  88. Singh R, Jamieson A, Cresswell P. 88.  2008. GILT is a critical host factor for Listeria monocytogenes infection. Nature 455:1244–47 [Google Scholar]
  89. Slade DJ, Lovelace LL, Chruszcz M, Minor W, Lebioda L, Sodetz JM. 89.  2008. Crystal structure of the MACPF domain of human complement protein C8α in complex with the C8γ subunit. J. Mol. Biol. 379:331–42 [Google Scholar]
  90. Soltani CE, Hotze EM, Johnson AE, Tweten RK. 90.  2007. Specific protein-membrane contacts are required for prepore and pore assembly by a cholesterol-dependent cytolysin. J. Biol. Chem. 282:15709–16 [Google Scholar]
  91. Soltani CE, Hotze EM, Johnson AE, Tweten RK. 91.  2007. Structural elements of the cholesterol-dependent cytolysins that are responsible for their cholesterol-sensitive membrane interactions. PNAS 104:20226–31 [Google Scholar]
  92. Sonnen AF, Plitzko JM, Gilbert RJ. 92.  2014. Incomplete pneumolysin oligomers form membrane pores. Open Biol. 4:140044 [Google Scholar]
  93. Stevens DL, Bryant AE. 93.  1993. Role of theta-toxin, a sulfhydryl-activated cytolysin, in the pathogenesis of clostridial gas gangrene. Clin. Infect. Dis. 16:S195–99 [Google Scholar]
  94. Stewart SE, D'Angelo ME, Piantavigna S, Tabor RF, Martin LL, Bird PI. 94.  2014. Assembly of streptolysin O pores assessed by quartz crystal microbalance and atomic force microscopy provides evidence for the formation of anchored but incomplete oligomers. Biochim. Biophys. Acta 1848:115–26 [Google Scholar]
  95. Tilley SJ, Orlova EV, Gilbert RJ, Andrew PW, Saibil HR. 95.  2005. Structural basis of pore formation by the bacterial toxin pneumolysin. Cell 121:247–56 [Google Scholar]
  96. Tweten RK. 96.  1988. Nucleotide sequence of the gene for perfringolysin O (theta-toxin) from Clostridium perfringens: significant homology with the genes for streptolysin O and pneumolysin. Infect. Immun. 56:3235–40 [Google Scholar]
  97. Wade KR, Hotze EM, Kuiper MJ, Morton CJ, Parker MW, Tweten RK. 97.  2015. An intermolecular electrostatic interaction controls the prepore to pore transition in a cholesterol-dependent cytolysin. PNAS 112:72204–9 [Google Scholar]
  98. Walker JA, Allen RL, Falmagne P, Johnson MK, Boulnois GJ. 98.  1987. Molecular cloning, characterization, and complete nucleotide sequence of the gene for pneumolysin, the sulfhydryl-activated toxin of Streptococcus pneumoniae. Infect. Immun. 55:1184–89 [Google Scholar]
  99. White SH, Wimley WC. 99.  1999. Membrane protein folding and stability: physical principles. Annu. Rev. Biophys. Biomol. Struct. 28:319–65 [Google Scholar]
  100. Wickham SE, Hotze EM, Farrand AJ, Polekhina G, Nero TL. 100.  et al. 2011. Mapping the intermedilysin-human CD59 receptor interface reveals a deep correspondence with the binding site on CD59 for complement binding proteins C8α and C9. J. Biol. Chem. 286:20952–62 [Google Scholar]
  101. Xu L, Huang B, Du H, Zhang XC, Xu J. 101.  et al. 2010. Crystal structure of cytotoxin protein suilysin from Streptococcus suis. Protein Cell 1:96–105 [Google Scholar]
/content/journals/10.1146/annurev-micro-091014-104233
Loading
The Unique Molecular Choreography of Giant Pore Formation by the Cholesterol-Dependent Cytolysins of Gram-Positive Bacteria
Annual Review of Microbiology 69, 323 (2015); https://doi.org/10.1146/annurev-micro-091014-104233
/content/journals/10.1146/annurev-micro-091014-104233
/content/journals/10.1146/annurev-micro-091014-104233
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error