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Chapter 11 : Injectosomes in Gram-Positive Bacteria

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Abstract:

Gram-positive bacteria are enclosed by a single membrane and therefore have apparently not evolved or acquired secretion systems similar to the type I, III, and IV systems found in the gram-negative bacteria. Although type III and IV systems are not found in gram-positive bacterial pathogens, these pathogens still translocate effectors into eukaryotic cells. This chapter examines the structure-function aspects of the cholesterol-dependent cytolysins (CDCs) and how the CDC mechanism has been adapted for use by to form its injectosome. The most recognizable feature of the CDC primary structure is the conserved undecapeptide that is located near the carboxy terminus of the CDCs. The CDCs are highly soluble proteins once released from the secretion system of the bacterial cell; and they undergo a remarkable transition that results in their conversion from soluble molecules into a supramolecular pore-forming membrane complex. The injectosome is composed of two known components, SLO and the Sec-dependent secretion pathway; in combination, they are necessary for the translocation of the NAD glycohydrolase (SPN) from into the cytoplasm of human keratinocytes. SPN is a 52-kDa protein that contains a typical signal peptide for a Sec-dependent protein and is found in the supernatant of cultured organisms. No SPN-related enzymes have been identified in other gram-positive bacteria, and SPN is not structurally related to any known protein. The injectosome of is a paradigm that will impact several areas of biology because of the many interesting questions posed by this system.

Citation: Tweten R, Caparon M. 2005. Injectosomes in Gram-Positive Bacteria, p 223-239. In Waksman G, Caparon M, Hultgren S (ed), Structural Biology of Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/9781555818395.ch11

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References

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1. Alouf, J. E., 1999. Introduction to the family of the structurally related cholesterol-binding cytolysins (‘sulfhydryl-activated toxins’), p. 443 456. In J. Alouf, and J. Freer (ed.), Bacterial Toxins: a Comprehensive Sourcebook. Academic Press, Ltd., London, United Kingdom.
2. Balachandran, P.,, S. K. Hollingshead,, J. C. Paton,, and D. E. Briles. 2001. The autolytic enzyme LytA of Streptococcus pneumoniae is not responsible for releasing pneumolysin. J. Bacteriol. 183: 3108 3116.
3. Bernheimer, A. W.,, P. D. Lazarides,, and A. T. Wilson. 1957. Diphosphopyridine nucleotidase as an extracellular product of streptococcal growth and its possible relationship to leukotoxicity. J. Exp. Med. 106: 27 37.
4. Bhakdi, S.,, M. Roth,, A. Sziegoleit,, and J. J. Tranum. 1984. Isolation and identification of two hemolytic forms of streptolysin-O. Infect. Immun. 46: 394 400.
5. Bhakdi, S.,, U. Weller,, I. Walev,, E. Martin,, D. Jonas,, and M. Palmer. 1993. A guide to the use of pore-forming toxins for controlled permeabilization of cell membranes. Med. Microbiol. Immunol. 182: 167 175.
6. Bielecki, J.,, P. Youngman,, P. Connelly,, and D. A. Portnoy. 1990. Bacillus subtilis expressing a haemolysin gene from Listeria monocytogenes can grow in mammalian cells. Nature 345: 175 176.
7. Billington, S. J.,, B. H. Jost,, W. A. Cuevas,, K. R. Bright,, and J. G. Songer. 1997. The Arcanobacterium (Actinomyces) pyogenes hemolysin, pyolysin, is a novel member of the thiol-activated cytolysin family. J. Bacteriol. 179: 6100 6106.
8. Bonev, B.,, R. Gilbert,, and A. Watts. 2000. Structural investigations of pneumolysin/lipid complexes. Mol. Membr. Biol. 17: 229 235.
9. Bonev, B. B.,, R. J. Gilbert,, P. W. Andrew,, O. Byron,, and A. Watts. 2001. Structural analysis of the protein/lipid complexes associated with pore formation by the bacterial toxin pneumolysin. J. Biol. Chem. 276: 5714 5719.
10. Bricker, A. L.,, C. Cywes,, C. D. Ashbaugh,, and M. R. Wessels. 2002. NAD +-glycohydrolase acts as an intracellular toxin to enhance the extracellular survival of group A streptococci. Mol. Microbiol. 44: 257 269.
11. Cossart, P. 2002. Molecular and cellular basis of the infection by Listeria monocytogenes:an overview. Int. J. Med. Microbiol. 291: 401 409.
12. Cossart, P.,, M. F. Vincente,, J. Mengaud,, F. Baquero,, J. C. Perez-Diaz,, and P. Berche. 1989. Listeriolysin O is essential for the virulence of Listeria monocytogenes:direct evidence obtained by gene complementation. Infect. Immun. 57: 3629 3639.
13. Decatur, A. L.,, and D. A. Portnoy. 2000. A PEST-like sequence in listeriolysin O essential for Listeria monocytogenes pathogenicity. Science 290: 992 995.
14. DeLano, W. L. 2002. The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, Calif.
15. Fang, Y.,, S. Cheley,, H. Bayley,, and J. Yang. 1997. The heptameric prepore of a staphylococcal alpha-hemolysin mutant in lipid bilayers imaged by atomic force microscopy. Biochemistry 36: 9518 9522.
16. Fehrenbach, F. J. 1972. NAD-glycohydrolase (streptolysin-O), ec 3225 and its role in cytolysis. Biochem. Biophys. Res. Commun. 48: 828 832.
17. Frehel, C.,, M. A. Lety,, N. Autret,, J. L. Beretti,, P. Berche,, and A. Charbit. 2003. Capacity of ivanolysin O to replace listeriolysin O in phagosomal escape and in vivo survival of Listeria monocytogenes. Microbiology 149: 611 620.
18. Galione, A. 1994. Cyclic ADP-ribose, the ADP-ribosyl cyclase pathway and calcium signalling. Mol. Cell. Endocrinol. 98: 125 131.
19. Galione, A.,, and G. C. Churchill. 2002. Interactions between calcium release pathways: multiple messengers and multiple stores. Cell Calcium 32: 343 354.
20. Giddings, K. S.,, A. E. Johnson,, and R. K. Tweten. 2003. Redefining cholesterol’s role in the mechanism of the cholesterol-dependent cytolysins. Proc. Natl. Acad. Sci. USA 100: 11315 11320.
21. Glomski, I. J.,, M. M. Gedde,, A. W. Tsang,, J. A. Swanson,, and D. A. Portnoy. 2002. The Listeria monocytogenes hemolysin has an acidic pH optimum to compartmentalize activity and prevent damage to infected host cells. J. Cell Biol. 156: 1029 1038.
22. Gouaux, J. E.,, O. Braha,, M. R. Hobaugh,, L. Song,, S. Cheley,, C. Shustak,, and H. Bayley. 1994. Subunit stoichiometry of staphylococcal alpha-hemolysin in crystals and on membranes: a heptameric transmembrane pore. Proc. Natl. Acad. Sci. USA 91: 12828 12831.
23. Greco, R.,, L. De Martino,, G. Donnarumma,, M. P. Conte,, L. Seganti,, and P. Valenti. 1995. Invasion of cultured human cells by Streptococcus pyogenes. Res. Microbiol. 146: 551 560.
24. Heuck, A. P.,, E. Hotze,, R. K. Tweten,, and A. E. Johnson. 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 1242.
25. Heuck, A. P.,, R. K. Tweten,, and A. E. Johnson. 2001. Beta-barrel pore-forming toxins: intriguing dimorphic proteins. Biochemistry 40: 9065 9073.
26. Heuck, A. P.,, R. K. Tweten,, and A. E. Johnson. 2003. Assembly and topography of the prepore complex in cholesterol- dependent cytolysins. J. Biol. Chem. 278: 31218 31225.
27. Hotze, E. M.,, A. P. Heuck,, D. M. Czajkowsky,, Z. Shao,, A. E. Johnson,, and R. K. Tweten. 2002. Monomermonomer interactions drive the prepore to pore conversion of a beta-barrel-forming cholesterol-dependent cytolysin. J. Biol. Chem. 277: 11597 11605.
28. Hotze, E. M.,, E. M. Wilson-Kubalek,, J. Rossjohn,, M. W. Parker,, A. E. Johnson,, and R. K. Tweten. 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 8268.
29. Iwamoto, M.,, I. Morita,, M. Fukuda,, S. Murota,, S. Ando,, and Y. Ohno-Iwashita. 1997. A biotinylated perfringolysin O derivative: a new probe for detection of cell surface cholesterol. Biochim. Biophys. Acta 1327: 222 230.
30. Iwamoto, M.,, M. Nakamura,, K. Mitsui,, S. Ando,, and Y. Ohno-Iwashita. 1993. Membrane disorganization induced by perfringolysin O (theta-toxin) of Clostridium perfringens—effect of toxin binding and selfassembly on liposomes. Biochim. Biophys. Acta 1153: 89 96.
31. Iwamoto, M.,, Y. Ohno-Iwashita,, and S. Ando. 1987. Role of the essential thiol group in the thiol-activated cytolysin from Clostridium perfringens. Eur. J. Biochem. 167: 425 430.
32. Iwamoto, M.,, Y. Ohno-Iwashita,, and S. Ando. 1990. Effect of isolated C-terminal fragment of theta-toxin (perfringolysin- O) on toxin assembly and membrane lysis. Eur. J. Biochem. 194: 25 31.
33. Jacobs, T.,, A. Darji,, N. Frahm,, M. Rohde,, J. Wehland,, T. Chakraborty,, and S. Weiss. 1998. Listeriolysin O: cholesterol inhibits cytolysis but not binding to cellular membranes. Mol. Microbiol. 28: 1081 1089.
34. Jones, S.,, and D. A. Portnoy. 1994. Characterization of Listeria monocytogenes pathogenesis in a strain expressing perfringolysin O in place of listeriolysin O. Infect. Immun. 62: 5608 5613.
35. Jones, S.,, K. Preiter,, and D. A. Portnoy. 1996. Conversion of an extracellular cytolysin into a phagosomespecific lysin which supports the growth of an intracellular pathogen. Mol. Microbiol. 21: 1219 1225.
36. Lee, H. C. 1994. Cyclic ADP-ribose: a new member of a super family of signalling cyclic nucleotides. Cell Signal 6: 591 600.
37. Lety, M. A.,, C. Frehel,, P. Berche,, and A. Charbit. 2002. Critical role of the N-terminal residues of listeriolysin O in phagosomal escape and virulence of Listeria monocytogenes. Mol. Microbiol. 46: 367 379.
38. Lety, M. A.,, C. Frehel,, I. Dubail,, J. L. Beretti,, S. Kayal,, P. Berche,, and A. Charbit. 2001. Identification of a PEST-like motif in listeriolysin O required for phagosomal escape and for virulence in Listeria monocytogenes. Mol. Microbiol. 39: 1124 1139.
39. Madden, J. C.,, N. Ruiz,, and M. Caparon. 2001. Cytolysin-mediated translocation (CMT): a functional equivalent of type III secretion in gram-positive bacteria. Cell 104: 143 152.
40. Miller, C. J.,, J. L. Elliot,, and R. L. Collier. 1999. Anthrax protective antigen: prepore-to-pore conversion. Biochemistry 38: 10432 10441.
41. Mobius, W.,, Y. Ohno-Iwashita,, E. G. van Donselaar,, V. M. Oorschot,, Y. Shimada,, T. Fujimoto,, H. F. Heijnen,, H. J. Geuze,, and J. W. Slot. 2002. Immunoelectron microscopic localization of cholesterol using biotinylated and non-cytolytic perfringolysin O. J. Histochem. Cytochem. 50: 43 55.
42. Nagamune, H.,, C. Ohnishi,, A. Katsuura,, K. Fushitani,, R. A. Whiley,, A. Tsuji,, and Y. Matsuda. 1996. Intermedilysin, a novel cytotoxin specific for human cells secreted by Streptococcus intermedius UNS46 isolated from a human liver abscess. Infect. Immun. 64: 3093 3100.
43. Nakamura, M.,, N. Sekino,, M. Iwamoto,, and Y. Ohno-Iwashita. 1995. Interaction of theta-toxin (perfringolysin O), a cholesterol-binding cytolysin, with liposomal membranes: change in the aromatic side chains upon binding and insertion. Biochemistry 34: 6513 6520.
44. Ohno-Iwashita, Y.,, M. Iwamoto,, S. Ando,, K. Mitsui,, and S. Iwashita. 1990. A modified θ-toxin produced by limited proteolysis and methylation: a probe for the functional study of membrane cholesterol. Biochim. Biophys. Acta 1023: 441 448.
45. Ohno-Iwashita, Y.,, M. Iwamoto,, K. Mitsui,, S. Ando,, and S. Iwashita. 1991. A cytolysin, theta-toxin, preferentially binds to membrane cholesterol surrounded by phospholipids with 18-carbon hydrocarbon chains in cholesterol-rich region. J. Biochem. 110: 369 375.
46. Ohno-Iwashita, Y.,, M. Iwamoto,, K. Mitsui,, S. Ando,, and Y. Nagai. 1988. Protease nicked q-toxin of Clostridium perfringens, a new membrane probe with no cytolytic effect, reveals two classes of cholesterol as toxin-binding sites on sheep erythrocytes. Eur. J. Biochem. 176: 95 101.
47. Olofsson, A.,, H. Hebert,, and M. Thelestam. 1993. The projection structure of perfringolysin-O ( Clostridium perfringens theta-toxin). FEBS Lett. 319: 125 127.
48. Palmer, M.,, R. Harris,, C. Freytag,, M. Kehoe,, J. Tranum-Jensen,, and S. Bhakdi. 1998. Assembly mechanism of the oligomeric streptolysin O pore: the early membrane lesion is lined by a free edge of the lipid membrane and is extended gradually during oligomerization. EMBO J. 17: 1598 1605.
49. Pinkney, M.,, E. Beachey,, and M. Kehoe. 1989. The thiol-activated toxin streptolysin O does not require a thiol group for activity. Infect. Immun. 57: 2553 2558.
50. Portnoy, D.,, P. S. Jacks,, and D. Hinrichs. 1988. The role of hemolysin for intracellular growth of Listeria monocytogenes. J. Exp. Med. 167: 1459 1471.
51. Portnoy, D. A.,, V. Auerbuch,, and I. J. Glomski. 2002. The cell biology of Listeria monocytogenes infection: the intersection of bacterial pathogenesis and cell-mediated immunity. J. Cell Biol. 158: 409 414.
52. Portnoy, D. A.,, R. K. Tweten,, M. Kehoe,, and J. Bielecki. 1992. The capacity of of listeriolysin O, streptolysin O, and perfringolysin O to mediate growth of Bacillus subtilis within mammalian cells. Infect. Immun. 60: 2710 2717.
53. Prigent, D.,, and J. E. Alouf. 1976. Interaction of streptolysin O with sterols. Biochem. Biophys. Acta 433: 422 428.
54. Ramachandran, R.,, A. P. Heuck,, R. K. Tweten,, and A. E. Johnson. 2002. Structural insights into the membrane- anchoring mechanism of a cholesterol-dependent cytolysin. Nat. Struct. Biol. 9: 823 827.
55. Rechsteiner, M.,, and S. W. Rogers. 1996. PEST sequences and regulation by proteolysis. Trends Biochem. Sci. 21: 267 271.
56. Rossjohn, J.,, S. C. Feil,, W. J. McKinstry,, R. K. Tweten,, and M. W. Parker. 1997. Structure of a cholesterolbinding thiol-activated cytolysin and a model of its membrane form. Cell 89: 685 692.
57. Rottem, S.,, R. M. Cole,, W. H. Habig,, M. F. Barile,, and M. C. Hardegree. 1982. Structural characteristics of tetanolysin and its binding to lipid vesicles. J. Bacteriol. 152: 888 892.
58. Ruiz, N.,, B. Wang,, A. Pentland,, and M. Caparon. 1998. Streptolysin O and adherence synergistically modulate proinflammatory responses of keratinocytes to group A streptococci. Mol. Microbiol. 27: 337 346.
59. Saunders, K. F.,, T. J. Mitchell,, J. A. Walker,, P. W. Andrew,, and G. J. Boulnois. 1989. Pneumolysin, the thiol-activated toxin of Streptococcus pneumoniae, does not require a thiol group for in vitro activity. Infect. Immun. 57: 2547 2552.
60. Scott, M. E.,, Z. Y. Dossani,, and M. Sandkvist. 2001. Directed polar secretion of protease from single cells of Vibrio cholerae via the type II secretion pathway. Proc. Natl. Acad. Sci. USA 98: 13978 13983.
61. Sekino-Suzuki, N.,, M. Nakamura,, K. I. Mitsui,, and Y. Ohno-Iwashita. 1996. Contribution of individual tryptophan residues to the structure and activity of theta-toxin (perfringolysin O), a cholesterol-binding cytolysin. Eur. J. Biochem. 241: 941 947.
62. Sellman, B. R.,, B. L. Kagan,, and R. K. Tweten. 1997. Generation of a membrane-bound, oligomerized pre-pore complex is necessary for pore formation by Clostridium septicum alpha toxin. Mol. Microbiol. 23: 551 558.
63. Shatursky, O.,, A. P. Heuck,, L. A. Shepard,, J. Rossjohn,, M. W. Parker,, A. E. Johnson,, and R. K. Tweten. 1999. The mechanism of membrane insertion for a cholesterol dependent cytolysin: a novel paradigm for pore-forming toxins. Cell 99: 293 299.
64. Shepard, L. A.,, A. P. Heuck,, B. D. Hamman,, J. Rossjohn,, M. W. Parker,, K. R. Ryan,, A. E. Johnson,, and R. K. Tweten. 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 14574.
65. Shepard, L. A.,, O. Shatursky,, A. E. Johnson,, and R. K. Tweten. 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 10293.
66. Shimada, Y.,, M. Maruya,, S. Iwashita,, and Y. Ohno-Iwashita. 2002. The C-terminal domain of perfringolysin O is an essential cholesterol-binding unit targeting to cholesterol-rich microdomains. Eur. J. Biochem. 269: 6195 6203.
67. Smith, G. A.,, H. Marquis,, S. Jones,, N. C. Johnston,, D. A. Portnoy,, and H. Goldfine. 1995. The two distinct phospholipases C of Listeria monocytogenes have overlapping roles in escape from a vacuole and cell-to-cell spread. Infect. Immun. 63: 4231 4237.
68. Song, P. I.,, Y. M. Park,, T. Abraham,, B. Harten,, A. Zivony,, N. Neparidze,, C. A. Armstrong,, and J. C. Ansel. 2002. Human keratinocytes express functional CD14 and toll-like receptor 4. J. Investig. Dermatol. 119: 424 432.
69. Stevens, D. L. 1996. Invasive group A streptococcal disease. Infect. Agents Dis. 5: 157 166.
70. Stevens, D. L.,, D. B. Salmi,, E. R. McIndoo,, and A. E. Bryant. 2000. Molecular epidemiology of nga and NAD glycohydrolase/ADP-ribosyltransferase activity among Streptococcus pyogenes causing streptococcal toxic shock syndrome. J. Infect. Dis. 182: 1117 1128.
71. Tweten, R. K.,, R. W. Harris,, and P. J. Sims. 1991. Isolation of a tryptic fragment from Clostridium perfringens θ-toxin that contains sites for membrane binding and self-aggregation. J. Biol. Chem. 266: 12449 12454.
72. Tweten, R. K.,, M. W. Parker,, and A. E. Johnson. 2001. The cholesterol-dependent cytolysins. Curr. Top. Microbiol. Immunol. 257: 15 33.
73. Wadsworth, S. J.,, and H. Goldfine. 2002. Mobilization of protein kinase C in macrophages induced by Listeria monocytogenes affects its internalization and escape from the phagosome. Infect. Immun. 70: 4650 4660.
74. Waheed, A. A.,, Y. Shimada,, H. F. Heijnen,, M. Nakamura,, M. Inomata,, M. Hayashi,, S. Iwashita,, J. W. Slot,, and Y. Ohno-Iwashita. 2001. Selective binding of perfringolysin O derivative to cholesterol-rich membrane microdomains (rafts). Proc. Natl. Acad. Sci. USA 98: 4926 4931.
75. Walev, I.,, M. Palmer,, A. Valeva,, U. Weller,, and S. Bhakdi. 1995. Binding, oligomerization, and pore formation by streptolysin O in erythrocytes and fibroblast membranes: detection of nonlytic polymers. Infect. Immun. 63: 1188 1194.
76. Walker, B.,, O. Braha,, S. Cheley,, and H. Bayley. 1995. An intermediate in the assembly of a pore-forming protein trapped with a genetically-engineered switch. Chem. Biol. 2: 99 105.
77. Walker, J. A.,, R. L. Allen,, P. Falmagne,, M. K. Johnson,, and G. J. Boulnois. 1987. Molecular cloning, characterization, and complete nucleotide sequence of the gene for pneumolysin, the sulfhydryl-activated toxin of Streptococcus pneumoniae. Infect. Immun. 55: 1184 1189.
78. Wang, B.,, N. Ruiz,, A. Pentland,, and M. Caparon. 1997. Keratinocyte proinflammatory responses to adherent and nonadherent group A streptococci. Infect. Immun. 65: 2119 2126.

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