Chapter 20 : Alternative Mechanisms of Protein Release

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This chapter reviews recent results concerning alternative strategies that strains employ to introduce proteins into the environment. The chapter is divided into three sections. The first section describes the cellular machinery comprising the type IV secretion system of . The second section discusses evidence that undergoes autolysis as a mechanism for releasing cytoplasmic proteins directly into the extracellular environment. The third section reviews recent data supporting the theory that cellular envelope proteins are released from via the formation of outer membrane vesicles, which appear to have the ability to be taken up into mammalian cells. The chapter focuses on the genes linked to the type IV secretion apparatus. On the basis of biochemical and genetic studies of the secretion apparatus, the locations of the six Cag proteins are predicted via analogy to their Vir homologs to be either part of the mating channel, or, alternatively, one of the putative ATPases. The presence of cytoplasmic proteins on the surface of the outer membrane both in vitro and in vivo is consistent with a mechanism of bacterial autolysis. In addition, the dependence of cytoplasmic protein release on the phase of bacterial growth in vitro suggests that the autolysis process is regulated. Bacterial autolysis probably involves mechanisms of peptidoglycan degradation to release cytoplasmic contents into the extracellular medium, which can then be strategically relocalized onto the outer membrane of other bacteria.

Citation: Blanke S, Ye D. 2001. Alternative Mechanisms of Protein Release, p 227-237. In Mobley H, Mendz G, Hazell S (ed), . ASM Press, Washington, DC. doi: 10.1128/9781555818005.ch20

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Type IV Secretion System Proteins
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Figure 1

homologs of the conjugation machine. (A) Genetic organization of the conjugation machine. type IV transporter components with homology to the Vir proteins are aligned underneath their homologs. (B) A model of the conjugation machine with the location of the homologs in (A) indicated by arrows with dashed lines. This model is compiled from biochemical data described in the text predicting both the localization and interactions of the individual Vir proteins.

Citation: Blanke S, Ye D. 2001. Alternative Mechanisms of Protein Release, p 227-237. In Mobley H, Mendz G, Hazell S (ed), . ASM Press, Washington, DC. doi: 10.1128/9781555818005.ch20
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Image of Figure 2
Figure 2

. altruistic autolysis. This model predicts that responds to specific environmental signals to activate genetically programmed bacterial autolysis. Specific protein autolysins degrade the peptidoglycan layer to lyse the cell envelope and release cytoplasmic proteins such as urease and catalase. Released urease is subsequently adsorbed to the surface of the neighboring bacteria and is important for survival in the acid environment and colonization of the gastric mucosa.

Citation: Blanke S, Ye D. 2001. Alternative Mechanisms of Protein Release, p 227-237. In Mobley H, Mendz G, Hazell S (ed), . ASM Press, Washington, DC. doi: 10.1128/9781555818005.ch20
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Figure 3

outer membrane vesicles budding. The release of outer membrane vesicles by is an alternative mechanism for the delivery of bacterial toxins and antigens to the gastric mucosa. These small vesicles are 50 to 300 nm in diameter. They contain VacA and other proteins such as porins within the trilayered membrane (OM, outer membrane; PS, periplasm; IM, inner membrane; C, cytoplasm).

Citation: Blanke S, Ye D. 2001. Alternative Mechanisms of Protein Release, p 227-237. In Mobley H, Mendz G, Hazell S (ed), . ASM Press, Washington, DC. doi: 10.1128/9781555818005.ch20
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1. Akopyants, N. S.,, S. W. Clifton,, D. Kersulyte,, J. E. Crabtree,, B. E. Youree,, C. A. Reece,, N. O. Bukanov,, E. S. Drazek,, B. A. Roe,, and D. E. Berg. 1998. Analyses of the cag pathogenicity island of Helicobacter pylori. Mol. Microbiol. 28:3753.
2. Alm, R. A.,, L. S. Ling,, D. T. Moir,, B. L. King,, E. D. Brown,, P. C. Doig,, D. R. Smith,, B. Noonan,, B. C. Guild,, B. L. deJonge,, G. Carmel,, P. J. Tummino,, A. Caruso,, M. Uria-Nickelsen,, D. M. Mills,, C. Ives,, R. Gibson,, D. Merberg,, S. D. Mills,, Q. Jiang,, D. E. Taylor,, G. F. Vovis,, and T. J. Trust. 1999. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397:176180.
3. Anderson, L.B.,, A. V. Hertzel,, and A. Das. 1996. Agrobacterium tumefaciens VirB7 and VirB9 form a disulfide-linked protein complex. Proc. Natl. Acad. Sci. USA 93:88898894.
4. Andersson, S. G.,, A. Zomorodipour,, J. O. Andersson,, T. Sicheritz-Ponten,, U. C. Alsmark,, R. M. Podowski,, A. K. Naslund,, A. S. Eriksson,, H. H. Winkler,, and C. G. Kurland. 1998. The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396:133140.
5. Bauerfeind, P.,, R. Garner,, B. E. Dunn,, and H. L. Mobley. 1997. Synthesis and activity of Helicobacter pylori urease and catalase at low pH. Gut 40:2530.
6. Beaupre, C. E.,, J. Bohne,, E. M. Dale,, and A. N. Binns. 1997. Interactions between VirB9 and VirBlO membrane proteins involved in movement of DNA from Agrobacterium tumefaciens into plant cells. J. Bacteriol. 179:7889.
7. Berry, A. M.,, J. C. Paton,, and D. Hansman. 1992. Effect of insertional inactivation of the genes encoding pneumolysin and autolysin on the virulence of Streptococcus pneumoniae type 3. Microb. Pathog. 12:8793.
8. Beveridge, T. J. 1999. Structures of gram-negative cell walls and their derived membrane vesicles. J. Bacteriol. 181: 47254733.
9. Beveridge, T. J.,, and J. L. Kadurugamuwa. 1996. Periplasm, periplasmic spaces, and their relation to bacterial wall structure: novel secretion of selected periplasmic proteins from Pseudomonas aeruginosa. Microb. Drug Resist. 2:18.
10. Binet, R.,, S. Letoffe,, J. M. Ghigo,, P. Delepelaire,, and C. Wandersman. 1997. Protein secretion by gram-negative bacterial ABC exporters—a review. Gene 192:711.
11. Blanchard, T. G.,, S. J. Czinn,, R. Maurer,, W. D. Thomas,, G. Soman,, and J. G. Nedrud. 1995. Urease-specific monoclonal antibodies prevent Helicobacter felis infection in mice. Infect. Immun. 63:13941399.
12. Blaser, M. 1998. Helicobacter pylori and gastric diseases. Br. Med. J. 316:15071510.
13. Blight, M. A.,, C. Chervaux,, and I. B. Holland. 1994. Protein secretion pathway in Escherichia coli. Curr. Opin. Biotechnol. 5:468474.
14. Bode, G.,, P. Malfertheiner,, G. Lehnhardt,, M. Nilius,, and H. Ditschuneit. 1993. Ultrastructural localization of urease of Helicobacter pylori. Med. Microbiol. Immunol. (Berlin) 182: 233242.
15. Buommino, E.,, F. Morelli,, S. Metafora,, F. Rossano,, B. Perfetto,, A. Baroni,, and M. A. Tufano. 1999. Porin from Pseudomonas aeruginosa induces apoptosis in an epithelial cell line derived from rat seminal vesicles. Infect. Immun. 67: 47944800.
16. Burns, D. L. 1999. Biochemistry of type IV secretion. Curr. Opin. Microbiol. 2:2529.
17. Censini, S.,, C. Lange,, Z. Xiang,, J. E. Crabtree,, P. Ghiara,, M. Borodovsky,, R. Rappuoli,, and A. Covacci. 1996. cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc. Natl. Acad. Sci. USA 93:1464814653.
18. China, B.,, and F. Goffaux. 1999. Secretion of virulence factors by Escherichia coli. Vet. Res. 30:181202.
19. Christie, P. J. 1997. Agrobacterium tumefaciens T-complex transport apparatus: a paradigm for a new family of multifunctional transporters in eubacteria. J. Bacteriol. 179: 30853094.
20. Christie, P. J.,, and J. P. Vogel. 2000. Bacterial type IV secretion: conjugation systems adapted to deliver effector molecules to host cells. Trends Microbiol. 8:354360.
21. Cover, T. 1999. Helicobacter pylori factors associated with disease. Gastroenterology 117:257261.
22. Dang, T. A.,, X. R. Zhou,, B. Graf,, and P. J. Christie. 1999. Dimerization of the Agrobacterium tumefaciens VirB4 ATPase and the effect of ATP-binding cassette mutations on the assembly and function of the T-DNA transporter. Mol. Microbiol. 32:12391253.
23. Das, A.,, and Y. H. Xie. 1998. Construction of transposon Tn3phoA: its application in defining the membrane topology of the Agrobacterium tumefaciens DNA transfer proteins. Mol. Microbiol. 27:405414.
24. Das, A.,, and Y. H. Xie. 2000. The Agrobacterium T-DNA transport pore proteins VirB8, VirB9, and VirBlO interact with one another. J. Bacteriol. 182:758763.
25. DeLoney, C. R.,, and N. L. Schiller. 1999. Competition of various beta-lactam antibiotics for the major penicillin-binding proteins of Helicobacter pylori: antibacterial activity and effects on bacterial morphology. Antimicrob. Agents Chemother. 43:27022709.
26.d'Enfert, C, I. Reyss, C. Wandersman, and A. P. Pugsley. 1989. Protein secretion by gram-negative bacteria. Characterization of two membrane proteins required for pullulanase secretion by Escherichia coli K-12. J. Biol. Chem. 264: 1746217468.
27. Dillard, J. P.,, and H. S. Selfert. 1997. A peptidoglycan hydrolase similar to bacteriophage endolysins acts as an autolysin in Neisseria gonorrhoeae. Mol. Microbiol. 25:893901.
28.Doidge, C, I. Crust, A. Lee, F. Buck, S. Hazell, and U. Manne. 1994. Therapeutic immunisation against Helicobacter infection. Lancet 343:914915. (Letter.)
29. Dore, M. P.,, D. Y. Graham,, and A. R. Sepulveda. 1999. Different penicillin-binding protein profiles in amoxicillin-resistant Helicobacter pylori. Helicobacter 4:154161.
30. Dubois, A.,, C. K. Lee,, N. Fiala,, H. Kleanthous,, P. T. Mehlman,, and T. Monath. 1998. Immunization against natural Helicobacter pylori infection in nonhuman primates. Infect. Immun. 66:43404346.
31. Dunn, B. E.,, H. Cohen,, and M. J. Blaser. 1997. Helicobacter pylori. Clin. Microbiol. Rev. 10:720741.
32. Dunn, B. E.,, and S. H. Phadnis. 1998. Structure, function and localization of Helicobacter pylori urease. Yale J. Biol. Med. 71:6373.
33. Dunn, B. E.,, N. B. Vakil,, B. G. Schneider,, M. M. Miller,, J. B. Zitzer,, T. Peutz,, and S. H. Phadnis. 1997. Localization of Helicobacter pylori urease and heat shock protein in human gastric biopsies. Infect. Immun. 65:11811188.
34. Falk, P. 2000. Theoretical and experimental approaches for studying factors defining the Helicobacter pylori-host relationship. Trends Microbiol. 8:321329.
35. Fernandez, D.,, G. M. Spudich,, X. R. Zhou,, and P.J. Christie. 1996. The Agrobacterium tumefaciens VirB7 lipoprotein is required for stabilization of VirB proteins during assembly of the T-complex transport apparatus. J. Bacteriol. 178: 31683176.
36. Fiocca, R.,, V. Necchi,, P. Sommi,, V. Ricci,, J. Telford,, T. L. Cover,, and E. Solcia. 1999. Release of Helicobacter pylori vacuolating cytotoxin by both a specific secretion pathway and budding of outer membrane vesicles. Uptake of released toxin and vesicles by gastric epithelium. J. Pathol. 188: 220226.
37. Frost, L. S.,, K. Ippen-Ihler,, and R. A. Skurray. 1994. Analysis of the sequence and gene products of the transfer region of the F sex factor. Microbiol Rev. 58:162210.
38. Garcia, J. L.,, J. M. Sanchez-Puelles,, P. Garcia,, R. Lopez,, C. Ronda,, and E. Garcia. 1986. Molecular characterization of an autolysin-defective mutant of Streptococcus pneumoniae. Biochem. Biophys. Res. Commun. 137:614619.
39. Genin, S.,, and C. A. Boucher. 1994. A superfamily of proteins involved in different secretion pathways in gram-negative bacteria: modular structure and specificity of the N-terminal domain. Mol. Gen. Genet. 243:112118.
40. Gennity, J. M.,, and M. Inouye. 1991. Protein secretion in bacteria. Curr. Opin. Biotechnol. 2:661667.
41. Guy, B.,, C. Hessler,, S. Fourage,, J. Haensler,, E. Vialon-Lafay,, B. Rokbi,, and M. J. Millet. 1998. Systemic immunization with urease protects mice against Helicobacter pylori infection. Vaccine 16:850856.
42. Hamilton, C. M.,, H. Lee,, P. L. Li,, D. M. Cook,, K. R. Piper,, S. B. von Bodman,, E. Lanka,, W. Ream,, and S. K. Farrand. 2000. TraG from RP4 and TraG and VirD4 from Ti plasmids confer relaxosome specificity to the conjugal transfer system of pTiC58. J. Bacteriol. 182:15411548.
43. Hansen, G.,, and M. D. Chilton. 1999. Lessons in gene transfer to plants by a gifted microbe. Curr. Top. Microbiol. Immunol. 240:2157.
44. Harris, A. G.,, S. L. Hazell,, and A. G. Netting. 2000. Use of digoxigenin-labelled ampicillin in the identification of penicillin-binding proteins in Helicobacter pylori. J. Antimicrob. Chemother. 45:591598.
45. Hirst, T. R.,, J. B. Hillary,, L. W. Ruddock,, and J. Yu. 1995. Translocation of folded proteins across bacterial outer membranes: a novel secretory phenomenon. Biochem. Soc. Trans. 23:985991.
46. Hirst, T. R.,, and R. A. Welch. 1988. Mechanisms for secretion of extracellular proteins by gram-negative bacteria. Trends Biochem. Sci. 13:265269.
47. Jacob-Dubuisson, F.,, M. Kuehn,, and S. J. Hultgren. 1993. A novel secretion apparatus for the assembly of adhesive bacterial pili. Trends Microbiol. 1:5055.
48. Kado, C.2000. On the mechanism of horizontal gene transfer by Agrobacterium tumefaciens, p. 6876. In Plant Genetic Engineering: towards the Third Millennium.
49.. Kadurugamuwa, J. L.,, and T. J. Beveridge. 1996. Bacteriolytic effect of membrane vesicles from Pseudomonas aeruginosa on other bacteria including pathogens: conceptually new antibiotics. J. Bacteriol. 178:27672774.
50. Kadurugamuwa, J. L.,, and T. J. Beveridge. 1997. Natural release of virulence factors in membrane vesicles by Pseudomonas aeruginosa and the effect of aminoglycoside antibiotics on their release. J. Antimicrob. Chemother. 40:615621.
51. Kadurugamuwa, J. L.,, and T. J. Beveridge. 1999. Membrane vesicles derived from Pseudomonas aeruginosa and Shigella flexneri can be integrated into the surfaces of other gram-negative bacteria. Microbiology 145:20512060.
52. Rolling, G. L.,, and K. R. Matthews. 1999. Export of virulence genes and Shiga toxin by membrane vesicles of Escherichia coli 0157:H7. Appl. Environ. Microbiol. 65:18431848.
53. Krause, S.,, M. Barcena,, W. Pansegrau,, R. Lurz,, J. M. Carazo,, and E. Lanka. 2000. Sequence-related protein export NTPases encoded by the conjugative transfer region of RP4 and by the cag pathogenicity island of Helicobacter pylori share similar hexameric ring structures. Proc. Natl. Acad. Sci. USA 97:30673072.
54. Krause, S.,, W. Pansegrau,, R. Lurz,, F. dela Cruz,, and E. Lanka. 2000. Enzymology of type IV macromolecule secretion systems: the conjugative transfer regions of plasmids RP4 and R388 and the cag pathogenicity island of Helicobacter pylori encode structurally and functionally related nucleoside triphosphate hydrolases. J. Bacteriol. 182:27612770.
55. Krishnamurthy, P.,, M. Parlow,, J. B. Zitzer,, N. B. Vakil,, H. L. Mobley,, M. Levy,, S. H. Phadnis,, and B. E. Dunn. 1998. Helicobacter pylori containing only cytoplasmic urease is susceptible to acid. Infect. Immun. 66:50605066.
56. Krishnamurthy, P.,, M. H. Parlow,, J. Schneider,, S. Burroughs,, C. Wickland,, N. B. Vakil,, B. E. Dunn,, and S. H. Phadnis. 1999. Identification of a novel penicillin-binding protein from Helicobacter pylori. J. Bacteriol. 181:51075110.
57. Lai, E. M.,, O. Chesnokova,, L. M. Banta,, and C. I. Kado. 2000. Genetic and environmental factors affecting T-pilin export and T-pilus biogenesis in relation to flagellation of Agrobacterium tumefaciens. J. Bacteriol. 182:37053716.
58. Lai, E. M.,, and C. I. Kado. 2000. The T-pilus of Agrobacterium tumefaciens. Trends Microbiol. 8:361369.
59. Lee, C. K.,, K. Soike,, J. Hill,, K. Georgakopoulos,, T. Tibbitts,, J. Ingrassia,, H. Gray,, J. Boden,, H. Kleanthous,, P. Giannasca,, T. Ermak,, R. Weltzin,, J. Blanchard,, and T. P. Monath. 1999. Immunization with recombinant Helicobacter pylori urease decreases colonization levels following experimental infection of rhesus monkeys. Vaccine 17:14931505.
60. Lewis, K. 2000. Programmed death in bacteria. Microbiol. Mol. Biol. Rev. 64:503514.
61. Li, P. L.,, I. Hwang,, H. Miyagi,, H. True,, and S. K. Farrand. 1999. Essential components of the Ti plasmid trb system, a type IV macromolecular transporter. J. Bacteriol. 181: 50335041.
62. Li, Z.,, A.J. Clarke,, and T.J. Beveridge. 1998. Gram-negative bacteria produce membrane vesicles which are capable of killing other bacteria. J. Bacteriol. 180:54785483.
63. Lory, S. 1992. Determinants of extracellular protein secretion in gram-negative bacteria. J. Bacteriol. 174:34233428.
64. Marchetti, M.,, B. Arico,, D. Burroni,, N. Figura,, R. Rappuoli,, and P. Ghiara. 1995. Development of a mouse model of Helicobacter pylori infection that mimics human disease. Science 267:16551658.
65. Marshall, B. J.,, L. J. Barrett,, C. Prakash,, R. W. McCallum,, and R. L. Guerrant. 1990. Urea protects Helicobacter (Campylobacter) pylori from the bactericidal effect of acid. Gastroenterology 99:697702.
66. Mayrand, D.,, and D. Grenier. 1989. Biological activities of outer membrane vesicles. Can. J. Microbiol. 35:607613.
67. Munzenmaier, A.,, C. Lange,, E. Glocker,, A. Covacci,, A. Moran,, S. Bereswill,, P. A. Baeuerle,, M. Kist,, and H. L. Pahl. 1997. A secreted/shed product of Helicobacter pylori activates transcription factor nuclear factor-kappa B. J. Immunol. 159:61406147.
68. Myers, G. A.,, T. H. Ermak,, K. Georgakopoulos,, T. Tibbits,, J. Ingrassia,, H. Gray,, H. Kleanthous,, C. K. Lee,, and T. P. Monath. 1999. Oral immunization with recombinant Helicobacter pylori urease confers long-lasting immunity against Helicobacter felis infection. Vaccine 17:13941403.
69. Novak, R.,, and E. Tuomanen. 1999. Pathogenesis of pneumococcal pneumonia. Semin. Respir. Infect. 14:209217.
70. Nunn, D. 1999. Bacterial type II protein export and pilus biogenesis: more than just homologies? Trends Cell Biol. 9: 402408.
71. O'Callaghan, D.,, C. Cazevieille,, A. Allardet-Servent,, M. L. Boschiroli,, G. Bourg,, V. Foulongne,, P. Frutos,, Y. Kulakov,, and M. Ramuz. 1999. A homologue of the Agrobacterium tumefaciens VirB and Bordetella pertussis Ptl type IV secretion systems is essential for intracellular survival of Brucella suis. Mol. Microbiol. 33:12101220.
72. Paton, J.C.,, P.W. Andrew,, G.J. Boulnois,andT.J.Mitchell. 1993. Molecular analysis of the pathogenicity of Streptococcus pneumoniae: the role of pneumococcal proteins. Annu. Rev. Microbiol. 47:89115.
73. Phadnis, S. H.,, M. H. Parlow,, M. Levy,, D. liver,, C. M. Caulkins,, J. B. Connors,, and B. E. Dunn. 1996. Surface localization of Helicobacter pylori urease and a heat shock protein homolog requires bacterial autolysis. Infect. Immun. 64: 905912.
74. Pugsley, A. P. 1993. The complete general secretory pathway in gram-negative bacteria. Microbiol. Rev. 57:50108.
75. Pugsley, A. P.,, C. d'Enfert,, I. Reyss,, and M. G. Kornacker. 1990. Genetics of extracellular protein secretion by gram-negative bacteria. Annu. Rev. Genet. 24:6790.
76. Radcliff, F. J.,, S. L. Hazell,, T. Kolesnikow,, C. Doidge,, and A. Lee. 1997. Catalase, a novel antigen for Helicobacter pylori vaccination. Infect. Immun. 65:46684674.
77. Rashkova, S.,, X. R. Zhou,, J. Chen,, and P. J. Christie. 2000. Self-assembly of the Agrobacterium tumefaciens VirB11 traffic ATPase. J. Bacteriol. 182:41374145.
78. Ream, W. 1998. Import of Agrobacterium tumefaciens virulence proteins and transferred DNA into plant cell nuclei. Subcell. Biochem. 29:365384.
79. Ronda, C.,, J. L. Garcia,, E. Garcia,, J. M. Sanchez-Puelles,, and R. Lopez. 1987. Biological role of the pneumococcal amidase. Cloning of the lytA gene in Streptococcus pneumoniae. Eur. J. Biochem. 164:621624.
80. Sandkvist, M.,, and M. Bagdasarian. 1996. Secretion of recombinant proteins by gram-negative bacteria. Curr. Opin. Biotechnol. 7:505511.
81. Schraw, W.,, M. S. McClain,, and T. L. Cover. 1999. Kinetics and mechanisms of extracellular protein release by Helicobacter pylori. Infect. Immun. 67:52475252.
82. Scott, D. R.,, D. Weeks,, C. Hong,, S. Postius,, K. Melchers,, and G. Sachs. 1998. The role of internal urease in acid resistance of Helicobacter pylori. Gastroenterology 114:5870.
83. Segal, G.,, J. J. Russo,, and H. A. Shuman. 1999. Relationships between a new type IV secretion system and the icm/dot virulence system of Legionella pneumophila. Mol. Microbiol. 34: 799809.
84. Shockman, G. D. 1992. The autolytic ('suicidase') system of Enterococcus hirae: from lysine depletion autolysis to biochemical and molecular studies of the two muramidases of Enterococcus hirae ATCC 9790. FEMS Microbiol Lett. 79: 261267.
85. Shockman, G. D.,, L. Daneo-Moore,, R. Kariyama,, and O. Massidda. 1996. Bacterial walls, peptidoglycan hydrolases, autolysins, and autolysis. Microb. Drug Resist. 2:9598.
86. Sipponen, P. 1998. Pathogenesis of the transformation from gastritis to malignancy. Aliment. Pharmacol. Ther. 12(Suppl.):6171.
87. Spudich, G. M.,, D. Fernandez,, X. R. Zhou,, and P. J. Christie. 1996. Intermolecular disulfide bonds stabilize VirB7 homodimers and VirB7/VirB9 heterodimers during biogenesis of the Agrobacterium tumefaciens T-complex transport apparatus. Proc. Natl. Acad. Sci. USA 93:75127517.
88. Stathopoulos, C.,, D. R. Hendrixson,, D. G. Thanassi,, S. J. Hultgren,, J. W. St. Geme 3rd,, and R. Curtiss 3rd . 2000. Secretion of virulence determinants by the general secretory pathway in gram-negative pathogens: an evolving story. Microb. Infect. 2:10611072.
89. Stein, M.,, R. Rappuoli,, and A. Covacci. 2000. Tyrosine phosphorylation of the Helicobacter pylori CagA antigen after cag-driven host cell translocation. Proc. Natl. Acad. Sci. USA 97:12631268.
90. Stephens, C. 1998. Protein secretion: getting folded proteins across membranes. Curr. Biol. 8:R578R581.
91. Stephens, K. M.,, C. Roush,, and E. Nester. 1995. Agrobacterium tumefaciens VirB11 protein requires a consensus nucleotide-binding site for function in virulence. J. Bacteriol. 177: 2736.
92. Tomb, J.-F.,, O. White,, A. R. Kerlavage,, R. A. Clayton,, G. G. Sutton,, R. D. Fleishmann,, K. A. Ketchum,, H. P. Klenk,, S. Gill,, B. A. Dougherty,, K. Nelson,, J. Quackenbush,, L. Zhou,, E. F. Kirkness,, S. Peterson,, B. Loftus,, D. Richardson,, R. Dodson,, H. G. Khalak,, A. Glodek,, K. McKenney,, L. M. Fitzegerald,, N. Lee,, M. D. Adams,, E. Hickey,, D. E. Berg,, J. D. Gocayne,, T. R. Utterback,, J. D. Peterson,, J. M. Kelley,, M. D. Cotton,, J. M. Weidman,, C. Fujii,, C. Bowman,, L. Wat-they,, E. Wallin,, W. S. Hayes,, M. Borodovsky,, P. D. Karp,, H. O. Smith,, C. M. Fraser,, and J. C. Venter. 1997. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388:539547.
93. Tummuru, M. K.,, S. A. Sharma,, and M. J. Blaser. 1995. Helicobacter pylori picB, a homologue of the Bordetella pertussis toxin secretion protein, is required for induction of IL-8 in gastric epithelial cells. Mol. Microbiol. 18:867876.
94. Vanet, A.,, and A. Labigne. 1998. Evidence for specific secretion rather than autolysis in the release of some Helicobacter pylori proteins. Infect. Immun. 66:10231027.
95. Vogel, J. P.,, H. L. Andrews,, S. K. Wong,, and R. R. Isberg. 1998. Conjugative transfer by the virulence system of Legionella pneumophila. Science 279:873876.
96. Wandersman, C. 1992. Secretion across the bacterial outer membrane. Trends Genet. 8:317322.
97. Williams, C. L.,, T. Preston,, M. Hossack,, C. Slater,, and K. E. McColl. 1996. Helicobacter pylori utilises urea for amino acid synthesis. FEMS Immunol. Med. Microbiol. 13:8794.
98. Winans, S. C.,, D. L. Burns,, and P. J. Christie. 1996. Adaptation of a conjugal transfer system for the export of pathogenic macromolecules. Trends Microbiol. 4:6468.
99. Zhou, L.,, R. Srisatjaluk,, D. E. Justus,, and R. J. Doyle. 1998. On the origin of membrane vesicles in gram-negative bacteria. FEMS Microbiol Lett. 163:223228.
100. Zhou, X. R.,, and P. J. Christie. 1997. Suppression of mutant phenotypes of the Agrobacterium tumefaciens VirB11 ATPase by overproduction of VirB proteins.J. Bacteriol. 179: 58355842.
101. Zupan, J.,, T. R. Muth,, O. Draper,, and P. Zambryski. 2000. The transfer of DNA from Agrobacterium tumefaciens into plants: a feast of fundamental insights. Plant J. 23:1128.
102. Zupan, J. R.,, D. Ward,, and P. Zambryski. 1998. Assembly of the VirB transport complex for DNA transfer from Agrobacterium tumefaciens to plant cells. Curr. Opin. Microbiol. 1:649655.


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Table 1

type IV system

Citation: Blanke S, Ye D. 2001. Alternative Mechanisms of Protein Release, p 227-237. In Mobley H, Mendz G, Hazell S (ed), . ASM Press, Washington, DC. doi: 10.1128/9781555818005.ch20

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