1887

Chapter 52 : Type II Protein Secretion and Twin-Arginine Translocation Promote the Pathogenesis of

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in
Zoomout

Type II Protein Secretion and Twin-Arginine Translocation Promote the Pathogenesis of , Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555815660/9781555813901_Chap52-1.gif /docserver/preview/fulltext/10.1128/9781555815660/9781555813901_Chap52-2.gif

Abstract:

Translocation of fully or partially folded proteins across bacterial membranes is a remarkable property of the type II secretion (T2S) system and the twin-arginine translocation (Tat) pathway. This chapter summarizes our current knowledge of the significance of T2S and Tat for . Mutational analysis showed that the secretion pathway (Lsp) promotes the secretion of at least 11 degradative enzymes, including acid phosphatases, chitinase, zinc-metalloprotease, ribonuclease, mono-, di-, triacylglycerol lipases, phospholipase A (PLA), lysophospholipases A (LPLA) and phospholipases C (PLC). Although all these strategies have been successful, they all have their limitation in defining the complete set of proteins secreted by the Lsp pathway. First, the genes encoding the secreted chitinase, ribonuclease, and tartrate-resistant acid phosphatase have not yet been identified. Second, genetic analysis indicates that some identified exoenzymes do not account for all the corresponding Lsp-dependent activity; e.g., supernatants of the plcA-negative strain retain 50% of the PLC activity of the wild type, indicating that there is more than one Lsp-secreted PLC. Finally, there are probably some additional Lsp-secreted proteins whose function has not been tested for. In conclusion, the Lsp system promotes the secretion of degradative enzymes, growth at low temperature, intracellular replication within amoebae and macrophages, as well as virulence in A/J mice. Moreover, the Tat pathway facilitates secretion of phospholipase C, cytochrome c–dependent respiration, growth in iron-limiting conditions, as well as intracellular replication. Further identification and characterization of Lsp and Tat substrates should therefore enhance our understanding of the pathogenesis of .

Citation: Rossier O, P. Cianciotto N. 2006. Type II Protein Secretion and Twin-Arginine Translocation Promote the Pathogenesis of , p 207-213. In Cianciotto N, Kwaik Y, Edelstein P, Fields B, Geary D, Harrison T, Joseph C, Ratcliff R, Stout J, Swanson M (ed), . ASM Press, Washington, DC. doi: 10.1128/9781555815660.ch52

Key Concept Ranking

Type IV Secretion Systems
0.41526258
0.41526258
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of FIGURE 1
FIGURE 1

Model for T2S by the Lsp system and its role in . Most type II exoproteins are synthesized with an N-terminal signal peptide that targets them to the general secretion pathway (Sec). Following translocation across the inner membrane, their signal peptide (triangle) is cleaved, and they can acquire some secondary structure in the periplasm. Proteins can then recruit the T2S, which spans the bacterial envelope, to cross the outer membrane. In , the T2S machinery is called Lsp for secretion pathway. It includes the ATPase LspE, the inner membrane protein LspF, the pseudopilin LspG, the prepilin peptidase PilD, and the outer membrane secretin LspD ( ). In , our mutagenesis studies have demonstrated that Lsp facilitates the secretion of degradative enzymes. In addition to influencing the morphology of colonies on agar plates, it also potentiates growth at low temperature. Finally, the Lsp pathway promotes intracellular infection in amoebae and human macrophages as well as virulence in the A/J mouse model of Legionnaires’ disease. OM, outer membrane; IM, inner membrane; Cyt, cytoplasm.

Citation: Rossier O, P. Cianciotto N. 2006. Type II Protein Secretion and Twin-Arginine Translocation Promote the Pathogenesis of , p 207-213. In Cianciotto N, Kwaik Y, Edelstein P, Fields B, Geary D, Harrison T, Joseph C, Ratcliff R, Stout J, Swanson M (ed), . ASM Press, Washington, DC. doi: 10.1128/9781555815660.ch52
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2
FIGURE 2

Model for Tat and its role in . Unlike the substrates of the Sec pathway, Tat substrates are folded prior to export across the cytoplasmic membrane. They are targeted to the Tat pathway by their amino-terminal signal peptide, which harbors twin arginines. The Tat machinery includes the inner membrane components TatA, TatB, and TatC. In , our mutagenesis studies have demonstrated that Tat facilitates the secretion of phospholipase C activity, cytochrome –dependent respiration, growth under low-iron conditions, and intracellular infection. Moreover it appears to promote biofilm formation ( ). OM, outer membrane; IM, inner membrane; Cyt, cytoplasm.

Citation: Rossier O, P. Cianciotto N. 2006. Type II Protein Secretion and Twin-Arginine Translocation Promote the Pathogenesis of , p 207-213. In Cianciotto N, Kwaik Y, Edelstein P, Fields B, Geary D, Harrison T, Joseph C, Ratcliff R, Stout J, Swanson M (ed), . ASM Press, Washington, DC. doi: 10.1128/9781555815660.ch52
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555815660.ch52
1. Aragon, V.,, S. Kurtz, and, N. P. Cianciotto. 2001. The Legionella pneumophila major acid phosphatase and its role in intracellular infection. Infect. Immun. 69:177185.
2. Aragon, V.,, S. Kurtz,, A. Flieger,, B. Neumeister, and, N. P. Cianciotto. 2000. Secreted enzymatic activities of wild-type and pilD-deficient Legionella pneumophila. Infect. Immun. 68:18551863.
3. Aragon, V.,, O. Rossier, and, N. P. Cianciotto. 2002. Legionella pneumophila genes that encode lipase and phospholipase C activities. Microbiology 148:22232231.
4. Banerji, S.,, M. Bewersdorff,, B. Hermes,, N. P. Cianciotto, and, A. Flieger. 2005. Characterization of the major secreted zinc metalloprotease-dependent glycerophospholipid:cholesterol acyl-transferase, PlaC, of Legionella pneumophila. Infect. Immun. 73:28992909.
5. Cianciotto, N. P. 2005. Type II secretion: a protein secretion system for all seasons. Trends Microbiol. 13:581588.
6. Conover, G. M.,, I. Derre,, J. P. Vogel, and, R. R. Isberg. 2003. The Legionella pneumophila LidA protein: a translocated substrate of the Dot/Icm system associated with maintenance of bacterial integrity. Mol. Microbiol. 48:305321.
7. De Buck, E.,, L. Maes,, E. Meyen,, L. Van Mel-laert,, N. Geukens,, J. Anne, and, E. Lammertyn. 2005. Legionella pneumophila Philadelphia-1 tatB and tatC affect intracellular replication and biofilm formation. Biochem. Biophys. Res. Commun. 331:14131420.
8. Dreyfus, L. A., and, B. H. Iglewski. 1986. Purification and characterization of an extracellular protease of Legionella pneumophila. Infect. Immun. 51:736743.
9. Flieger, A.,, S. Gong,, M. Faigle,, S. Stevanovic,, N. P. Cianciotto, and, B. Neumeister. 2001. Novel lysophospholipase A secreted by Legionella pneumophila. J. Bacteriol. 183:21212124.
10. Flieger, A.,, B. Neumeister, and, N. P. Cianciotto. 2002. Characterization of the gene encoding the major secreted lysophospholipase A of Legionella pneumophila and its role in detoxification of lysophosphatidylcholine. Infect. Immun. 70:60946106.
11. Hales, L. M., and, H. A. Shuman. 1999. Legionella pneumophila contains a type II general secretion pathway required for growth in amoebae as well as for secretion of the Msp protease. Infect. Immun. 67:36623666.
12. Moffat, J. F.,, P. H. Edelstein,, D. P. Regula, Jr.,, J. D. Cirillo, and, L. S. Tompkins. 1994. Effects of an isogenic Zn-metalloprotease-deficient mutant of Legionella pneumophila in a guinea-pig pneumonia model. Mol. Microbiol. 12:693705.
13. Palmer, T., and, B. C. Berks. 2003. Moving folded proteins across the bacterial cell membrane. Microbiol. 149:547556.
14. Polesky, A. H.,, J. T. Ross,, S. Falkow, and, L. S. Tompkins. 2001. Identification of Legionella pneumophila genes important for infection of amoebas by signature-tagged mutagenesis. Infect. Immun. 69:977987.
15. Quinn, F. D., and, L. S. Tompkins. 1989. Analysis of a cloned sequence of Legionella pneumophila encoding a 38 kD metalloprotease possessing haemolytic and cytotoxic activities. Mol. Microbiol. 3:797805.
16. Rossier, O., and, N. P. Cianciotto. 2005. The Legionella pneumophila tatB gene facilitates secretion of phospholipase C, growth under iron-limiting conditions, and intracellular infection. Infect. Im-mun. 73:20202032.
17. Rossier, O., and, N. P. Cianciotto. 2001. Type II protein secretion is a subset of the PilD-dependent processes that facilitate intracellular infection by Legionella pneumophila. Infect. Immun. 69:20922098.
18. Rossier, O.,, S. R. Starkenburg, and, N. P. Cianciotto. 2004. Legionella pneumophila type II protein secretion promotes virulence in the A/J mouse model of Legionnaires’ disease pneumonia. Infect. Immun. 72:310321.
19. Soderberg, M. A.,, O. Rossier, and, N. P. Cianciotto. 2004. The type II protein secretion system of Legionella pneumophila promotes growth at low temperatures. J. Bacteriol. 186:37123720.
20. Swanson, M. S., and, B. K. Hammer. 2000. Legionella pneumophila pathogenesis: a fateful journey from amoebae to macrophages. Annu. Rev. Microbiol. 54:567613.
21. Szeto, L., and, H. A. Shuman. 1990. The Legionella pneumophila major secretory protein, a protease, is not required for intracellular growth or cell killing. Infect. Immun. 58:25852592.
22. Zink, S. D.,, L. Pedersen,, N. P. Cianciotto, and, Y. Abu-Kwaik. 2002. The Dot/Icm type IV secretion system of Legionella pneumophila is essential for the induction of apoptosis in human macrophages. Infect. Immun. 70:16571663.

Tables

Generic image for table
TABLE 1

Secreted enzymatic activities promoted by Lsp

Citation: Rossier O, P. Cianciotto N. 2006. Type II Protein Secretion and Twin-Arginine Translocation Promote the Pathogenesis of , p 207-213. In Cianciotto N, Kwaik Y, Edelstein P, Fields B, Geary D, Harrison T, Joseph C, Ratcliff R, Stout J, Swanson M (ed), . ASM Press, Washington, DC. doi: 10.1128/9781555815660.ch52

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error