Abstract
Legionella pneumophila is an opportunistic pathogen responsible for Legionnaires’ disease. This bacterium survives and replicates within phagocytes by bypassing their bactericidal activity. Intracellular replication of L. pneumophila requires the Dot/Icm type IV secretion system made of approximately 27 proteins that presumably traverses the bacterial and phagosomal membranes. The perturbation of the host killing ability largely is mediated by the collective functions of the protein substrates injected into host cells via the Dot/Icm transporter. Proper protein translocation by Dot/Icm is determined by a number of factors, including signals recognizable by the translocator, chaperones that may facilitate the proper folding of substrates and transcriptional regulation and protein stability that determine the abundance and temporal transfer of the substrates. Although a large number of Dot/Icm substrates have been identified, investigation to understand the translocation is ongoing. Here we summarized the recent advancements in our understanding of the factors that determine the protein translocation activity of the Dot/Icm transporter.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- Dot/Icm:
-
Defective in organelle trafficking/intracellular multiplication)
- Arf:
-
ADP ribosylation factor
- GEFs:
-
Guanine nucleotide exchange factors
References
Abu Kwaik Y, Gao LY, Stone BJ, Venkataraman C, Harb OS (1998) Appl Environ Microbiol 64:3127–3133
Altman E, Segal G (2008) J Bacteriol 190:1985–1996
Bardill JP, Miller JL, Vogel JP (2005) Mol Microbiol 56:90–103
Beare PA, Gilk SD, Larson CL, Hill J, Stead CM, Omsland A, Cockrell DC, Howe D, Voth DE, Heinzen RA (2011) MBio 2:e00175–11
Belyi Y, Niggeweg R, Opitz B, Vogelsgesang M, Hippenstiel S, Wilm M, Aktories K (2006) Proc Natl Acad Sci U S A 103:16953–16958
Belyi Y, Tabakova I, Stahl M, Aktories K (2008) J Bacteriol 190:3026–3035
Berger KH, Isberg RR (1993) Mol Microbiol 7:7–19
Brand BC, Sadosky AB, Shuman HA (1994) Mol Microbiol 14:797–808
Burstein D, Zusman T, Degtyar E, Viner R, Segal G, Pupko T (2009) PLoS Pathog 5:e1000508
Buscher BA, Conover GM, Miller JL, Vogel SA, Meyers SN, Isberg RR, Vogel JP (2005) J Bacteriol 187:2927–2938
Cambronne ED, Roy CR (2007) PLoS Pathog 3:e188
Campodonico EM, Chesnel L, Roy CR (2005) Mol Microbiol 56:918–933
Carey KL, Newton HJ, Luhrmann A, Roy CR (2011) PLoS Pathog 7:e1002056
Cazalet C, Rusniok C, Bruggemann H, Zidane N, Magnier A, Ma L, Tichit M, Jarraud S, Bouchier C, Vandenesch F, Kunst F, Etienne J, Glaser P, Buchrieser C (2004) Nat Genet 36:1165–1173
Charpentier X, Gabay JE, Reyes M, Zhu JW, Weiss A, Shuman HA (2009) PLoS Pathog 5:e1000501
Chen J, de Felipe KS, Clarke M, Lu H, Anderson OR, Segal G, Shuman HA (2004) Science 303:1358–1361
Chien M, Morozova I, Shi S, Sheng H, Chen J, Gomez SM, Asamani G, Hill K, Nuara J, Feder M, Rineer J, Greenberg JJ, Steshenko V, Park SH, Zhao B, Teplitskaya E, Edwards JR, Pampou S, Georghiou A, Chou IC, Iannuccilli W, Ulz ME, Kim DH, Geringer-Sameth A, Goldsberry C, Morozov P, Fischer SG, Segal G, Qu X, Rzhetsky A, Zhang P, Cayanis E, De Jong PJ, Ju J, Kalachikov S, Shuman HA, Russo JJ (2004) Science 305:1966–1968
Coers J, Kagan JC, Matthews M, Nagai H, Zuckman DM, Roy CR (2000) Mol Microbiol 38:719–736
Conover GM, Derre I, Vogel JP, Isberg RR (2003) Mol Microbiol 48:305–321
de Felipe KS, Pampou S, Jovanovic OS, Pericone CD, Ye SF, Kalachikov S, Shuman HA (2005) J Bacteriol 187:7716–7726
Degtyar E, Zusman T, Ehrlich M, Segal G (2009) Cell Microbiol 11:1219–1235
Diederen BM (2008) J Infect 56:1–12
Dolezal P, Aili M, Tong J, Jiang JH, Marobbio CM, Lee SF, Schuelein R, Belluzzo S, Binova E, Mousnier A, Frankel G, Giannuzzi G, Palmieri F, Gabriel K, Naderer T, Hartland EL, Lithgow T (2012) PLoS Pathog 8:e1002459
Fattori J, Prando A, Martins AM, Rodrigues FH, Tasic L (2011) Protein Pept Lett 18:158–166
Fields BS, Benson RF, Besser RE (2002) Clin Microbiol Rev 15:506–526
Fontana MF, Banga S, Barry KC, Shen X, Tan Y, Luo ZQ, Vance RE (2011) PLoS Pathog 7:e1001289
Fraser DW, Tsai TR, Orenstein W, Parkin WE, Beecham HJ, Sharrar RG, Harris J, Mallison GF, Martin SM, McDade JE, Shepard CC, Brachman PS (1977) N Engl J Med 297:1189–1197
Gal-Mor O, Segal G (2003a) J Bacteriol 185:4908–4919
Gal-Mor O, Segal G (2003b) Microb Pathog 34:187–194
Gal-Mor O, Zusman T, Segal G (2002) J Bacteriol 184:3823–3833
Gomez-Valero L, Rusniok C, Cazalet C, Buchrieser C (2011) Front Microbiol 2:208
Gomis-Ruth FX, Moncalian G, Perez-Luque R, Gonzalez A, Cabezon E, de la Cruz F, Coll M (2001) Nature 409:637–641
Gomis-Ruth FX, Sola M, de la Cruz F, Coll M (2004) Curr Pharm Des 10:1551–1565
Hammer BK, Tateda ES, Swanson MS (2002) Mol Microbiol 44:107–118
Huang L, Boyd D, Amyot WM, Hempstead AD, Luo ZQ, O’Connor TJ, Chen C, Machner M, Montminy T, Isberg RR (2010) Cell Microbiol 13:227–245
Hubber A, Roy CR (2010) Annu Rev Cell Dev Biol 26:261–283
Isberg RR, O’Connor TJ, Heidtman M (2009) Nat Rev Microbiol 7:13–24
Judd PK, Kumar RB, Das A (2005) Proc Natl Acad Sci U S A 102:11498–11503
Jules M, Buchrieser C (2007) FEBS Lett 581:2829–2838
Komano T, Yoshida T, Narahara K, Furuya N (2000) Mol Microbiol 35:1348–1359
Kubori T, Hyakutake A, Nagai H (2008) Mol Microbiol 67:1307–1319
Kubori T, Shinzawa N, Kanuka H, Nagai H (2010) PLoS Pathog 6:e1001216
Lifshitz Z, Burstein D, Peeri M, Zusman T, Schwartz K, Shuman HA, Pupko T, Segal G (2013) Proc Natl Acad Sci U S A 110:E707–E715
Liu Y, Gao P, Banga S, Luo ZQ (2008) Proc Natl Acad Sci U S A 105:9385–9390
Liu Y, Luo ZQ (2007) Infect Immun 75:592–603
Luo ZQ (2011) Front Microbiol 2:31
Luo ZQ, Isberg RR (2004) Proc Natl Acad Sci U S A 101:841–846
Molofsky AB, Swanson MS (2004) Mol Microbiol 53:29–40
Nagai H, Cambronne ED, Kagan JC, Amor JC, Kahn RA, Roy CR (2005) Proc Natl Acad Sci U S A 102:826–831
Nagai H, Kagan JC, Zhu X, Kahn RA, Roy CR (2002) Science 295:679–682
Nagai H, Kubori T (2011) Front Microbiol 2:136
Neunuebel MR, Chen Y, Gaspar AH, Backlund PS Jr, Yergey A, Machner MP (2011) Science 333:453–456
Ninio S, Celli J, Roy CR (2009) PLoS Pathog 5:e1000278
O’Connor TJ, Adepoju Y, Boyd D, Isberg RR (2011) Proc Natl Acad Sci U S A 108:14733–14740
O’Connor TJ, Boyd D, Dorer MS, Isberg RR (2012) Science 338:1440–1444
Rolando M, Sanulli S, Rusniok C, Gomez-Valero L, Bertholet C, Sahr T, Margueron R, Buchrieser C (2013) Cell Host Microbe 13:395–405
Schroeder GN, Petty NK, Mousnier A, Harding CR, Vogrin AJ, Wee B, Fry NK, Harrison TG, Newton HJ, Thomson NR, Beatson SA, Dougan G, Hartland EL, Frankel G (2010) J Bacteriol 192:6001–6016
Segal G, Purcell M, Shuman HA (1998) Proc Natl Acad Sci U S A 95:1669–1674
Segal G, Shuman HA (1997) Infect Immun 65:5057–5066
Segal G, Shuman HA (1999) Infect Immun 67:2117–2124
Sexton JA, Miller JL, Yoneda A, Kehl-Fie TE, Vogel JP (2004) Infect Immun 72:5983–5992
Sexton JA, Yeo HJ, Vogel JP (2005) Mol Microbiol 57:70–84
Shen X, Banga S, Liu Y, Xu L, Gao P, Shamovsky I, Nudler E, Luo ZQ (2009) Cell Microbiol 11:911–926
Shohdy N, Efe JA, Emr SD, Shuman HA (2005) Proc Natl Acad Sci U S A 102:4866–4871
Sutherland MC, Nguyen TL, Tseng V, Vogel JP (2012) PLoS Pathog 8:e1002910
Swanson MS, Isberg RR (1996) Infect Immun 64:2585–2594
Tan Y, Arnold RJ, Luo ZQ (2011) Proc Natl Acad Sci U S A 108:21212–21217
Tan Y, Luo ZQ (2011) Nature 475:506–509
Thanassi DG, Bliska JB, Christie PJ (2012) FEMS Microbiol Rev 36:1046–1082
Tilney LG, Harb OS, Connelly PS, Robinson CG, Roy CR (2001) J Cell Sci 114:4637–4650
VanRheenen SM, Dumenil G, Isberg RR (2004) Infect Immun 72:5972–5982
Vergunst AC, Schrammeijer B, den Dulk-Ras A, de Vlaam CM, Regensburg-Tuink TJ, Hooykaas PJ (2000) Science 290:979–982
Vincent CD, Buscher BA, Friedman JR, Williams LA, Bardill P, Vogel JP (2006a) J Bacteriol 188:8231–8243
Vincent CD, Friedman JR, Jeong KC, Buford EC, Miller JL, Vogel JP (2006b) Mol Microbiol 62:1278–1291
Vincent CD, Vogel JP (2006) Mol Microbiol 61:596–613
Vogel JP, Andrews HL, Wong SK, Isberg RR (1998) Science 279:873–876
Vogel JP, Isberg RR (1999) Curr Opin Microbiol 2:30–34
Wilkins BM, Thomas AT (2000) Mol Microbiol 38:650–657
Xu L, Luo ZQ (2013) Microbes Infect 15:157–167
Xu L, Shen X, Bryan A, Banga S, Swanson MS, Luo ZQ (2010) PLoS Pathog 6:e1000822
Zhu W, Banga S, Tan Y, Zheng C, Stephenson R, Gately J, Luo ZQ (2011) PLoS ONE 6:e17638
Zusman T, Degtyar E, Segal G (2008) Infect Immun 76:4581–4591
Zusman T, Feldman M, Halperin E, Segal G (2004) Infect Immun 72:3398–3409
Acknowledgments
We thank Dr. Xiaodi Niu (Jilin University, Changchun, China) for help in the preparation of the figure and members of our laboratory for helpful discussion. Our work was supported by NIH-NIAID grants R01AI069344, K02AI085403 and R21AI092043.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Qiu, J., Luo, ZQ. (2013). Effector Translocation by the Legionella Dot/Icm Type IV Secretion System. In: Hilbi, H. (eds) Molecular Mechanisms in Legionella Pathogenesis. Current Topics in Microbiology and Immunology, vol 376. Springer, Berlin, Heidelberg. https://doi.org/10.1007/82_2013_345
Download citation
DOI: https://doi.org/10.1007/82_2013_345
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-40590-7
Online ISBN: 978-3-642-40591-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)