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Protein secretion systems in bacterial pathogens |
Li XU1,*(),Yancheng LIU2,*() |
1. Weill Institute for Cell and Molecular Biology, Cornell University, Ithaca, NY 14853, USA 2. Department of Microbiology and Immunology, Cornell University, Ithaca, NY 14853, USA |
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Abstract Many bacterial pathogens utilize specialized secretion systems to deliver virulence factors into the extracellular milieu. These exported effectors act to manipulate various processes of targeted cells in order to create a suitable niche for bacterial growth. Currently, seven different types of secretion system have been described, of which Type I – VI are mainly present in Gram-negative bacteria and the newly discovered Type VII system seems exclusive to Gram-positive species. This review summaries our current understanding on the architecture and transport mechanisms of each secretion apparatus. We also discuss recent studies revealing the roles that these secretion systems and their substrates play in microbial pathogenesis.
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Keywords
bacterial pathogen
secretion system
virulence factors
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Corresponding Author(s):
Li XU
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Just Accepted Date: 25 September 2014
Online First Date: 14 November 2014
Issue Date: 13 January 2015
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1 |
Abdallah A M, Verboom T, Hannes F, Safi M, Strong M, Eisenberg D, Musters R J, Vandenbroucke-Grauls C M, Appelmelk B J, Luirink J, Bitter W (2006). A specific secretion system mediates PPE41 transport in pathogenic mycobacteria. Mol Microbiol, 62(3): 667–679
https://doi.org/10.1111/j.1365-2958.2006.05409.x
pmid: 17076665
|
2 |
Abdallah A M, Verboom T, Weerdenburg E M, Gey van Pittius N C, Mahasha P W, Jiménez C, Parra M, Cadieux N, Brennan M J, Appelmelk B J, Bitter W (2009). PPE and PE_PGRS proteins of Mycobacterium marinum are transported via the type VII secretion system ESX-5. Mol Microbiol, 73(3): 329–340
https://doi.org/10.1111/j.1365-2958.2009.06783.x
pmid: 19602152
|
3 |
Anderson M, Chen Y H, Butler E K, Missiakas D M (2011). EsaD, a secretion factor for the Ess pathway in Staphylococcus aureus. J Bacteriol, 193(7): 1583–1589
https://doi.org/10.1128/JB.01096-10
pmid: 21278286
|
4 |
Aschtgen M S, Gavioli M, Dessen A, Lloubès R, Cascales E (2010). The SciZ protein anchors the enteroaggregative Escherichia coli Type VI secretion system to the cell wall. Mol Microbiol, 75(4): 886–899
https://doi.org/10.1111/j.1365-2958.2009.07028.x
pmid: 20487285
|
5 |
Atmakuri K, Cascales E, Christie P J (2004). Energetic components VirD4, VirB11 and VirB4 mediate early DNA transfer reactions required for bacterial type IV secretion. Mol Microbiol, 54(5): 1199–1211
https://doi.org/10.1111/j.1365-2958.2004.04345.x
pmid: 15554962
|
6 |
Backert S, Meyer T F (2006). Type IV secretion systems and their effectors in bacterial pathogenesis. Curr Opin Microbiol, 9(2): 207–217
https://doi.org/10.1016/j.mib.2006.02.008
pmid: 16529981
|
7 |
Bandyopadhyay P, Liu S, Gabbai C B, Venitelli Z, Steinman H M (2007). Environmental mimics and the Lvh type IVA secretion system contribute to virulence-related phenotypes of Legionella pneumophila. Infect Immun, 75(2): 723–735
https://doi.org/10.1128/IAI.00956-06
pmid: 17101653
|
8 |
Baptista C, Barreto H C, S?o-José C (2013). High levels of DegU-P activate an Esat-6-like secretion system in Bacillus subtilis. PLoS ONE, 8(7): e67840
https://doi.org/10.1371/journal.pone.0067840
pmid: 23861817
|
9 |
Bardill J P, Miller J L, Vogel J P (2005). IcmS-dependent translocation of SdeA into macrophages by the Legionella pneumophila type IV secretion system. Mol Microbiol, 56(1): 90–103
https://doi.org/10.1111/j.1365-2958.2005.04539.x
pmid: 15773981
|
10 |
Basler M, Pilhofer M, Henderson G P, Jensen G J, Mekalanos J J (2012). Type VI secretion requires a dynamic contractile phage tail-like structure. Nature, 483(7388): 182–186
https://doi.org/10.1038/nature10846
pmid: 22367545
|
11 |
Berks B C (1996). A common export pathway for proteins binding complex redox cofactors? Mol Microbiol, 22(3): 393–404
https://doi.org/10.1046/j.1365-2958.1996.00114.x
pmid: 8939424
|
12 |
Berks B C, Palmer T, Sargent F (2005). Protein targeting by the bacterial twin-arginine translocation (Tat) pathway. Curr Opin Microbiol, 8(2): 174–181
https://doi.org/10.1016/j.mib.2005.02.010
pmid: 15802249
|
13 |
Bernardini M L, Mounier J, d’Hauteville H, Coquis-Rondon M, Sansonetti P J (1989). Identification of icsA, a plasmid locus of Shigella flexneri that governs bacterial intra- and intercellular spread through interaction with F-actin. Proc Natl Acad Sci USA, 86(10): 3867–3871
https://doi.org/10.1073/pnas.86.10.3867
pmid: 2542950
|
14 |
Birtalan S C, Phillips R M, Ghosh P (2002). Three-dimensional secretion signals in chaperone-effector complexes of bacterial pathogens. Mol Cell, 9(5): 971–980
https://doi.org/10.1016/S1097-2765(02)00529-4
pmid: 12049734
|
15 |
Blocker A, Jouihri N, Larquet E, Gounon P, Ebel F, Parsot C, Sansonetti P, Allaoui A (2001). Structure and composition of the Shigella flexneri “needle complex”, a part of its type III secreton. Mol Microbiol, 39(3): 652–663
https://doi.org/10.1046/j.1365-2958.2001.02200.x
pmid: 11169106
|
16 |
B?nemann G, Pietrosiuk A, Diemand A, Zentgraf H, Mogk A (2009). Remodelling of VipA/VipB tubules by ClpV-mediated threading is crucial for type VI protein secretion. EMBO J, 28(4): 315–325
https://doi.org/10.1038/emboj.2008.269
pmid: 19131969
|
17 |
Boyer F, Fichant G, Berthod J, Vandenbrouck Y, Attree I (2009). Dissecting the bacterial type VI secretion system by a genome wide in silico analysis: what can be learned from available microbial genomic resources? BMC Genomics, 10(1): 104
https://doi.org/10.1186/1471-2164-10-104
pmid: 19284603
|
18 |
Brodin P, Majlessi L, Marsollier L, de Jonge M I, Bottai D, Demangel C, Hinds J, Neyrolles O, Butcher P D, Leclerc C, Cole S T, Brosch R (2006). Dissection of ESAT-6 system 1 of Mycobacterium tuberculosis and impact on immunogenicity and virulence. Infect Immun, 74(1): 88–98
https://doi.org/10.1128/IAI.74.1.88-98.2006
pmid: 16368961
|
19 |
Brooks T M, Unterweger D, Bachmann V, Kostiuk B, Pukatzki S (2013). Lytic activity of the Vibrio cholerae type VI secretion toxin VgrG-3 is inhibited by the antitoxin TsaB. J Biol Chem, 288(11): 7618–7625
https://doi.org/10.1074/jbc.M112.436725
pmid: 23341465
|
20 |
Burkinshaw B J, Strynadka N C (2014). Assembly and structure of the T3SS. Biochim Biophys Acta, 1843(8): 1649–1663
https://doi.org/10.1016/j.bbamcr.2014.01.035
pmid: 24512838
|
21 |
Burts M L, DeDent A C, Missiakas D M (2008). EsaC substrate for the ESAT-6 secretion pathway and its role in persistent infections of Staphylococcus aureus. Mol Microbiol, 69(3): 736–746
https://doi.org/10.1111/j.1365-2958.2008.06324.x
pmid: 18554323
|
22 |
Burts M L, Williams W A, DeBord K, Missiakas D M (2005). EsxA and EsxB are secreted by an ESAT-6-like system that is required for the pathogenesis of Staphylococcus aureus infections. Proc Natl Acad Sci USA, 102(4): 1169–1174
https://doi.org/10.1073/pnas.0405620102
pmid: 15657139
|
23 |
Buscher B A, Conover G M, Miller J L, Vogel S A, Meyers S N, Isberg R R, Vogel J P (2005). The DotL protein, a member of the TraG-coupling protein family, is essential for viability of Legionella pneumophila strain Lp02. J Bacteriol, 187(9): 2927–2938
https://doi.org/10.1128/JB.187.9.2927-2938.2005
pmid: 15838018
|
24 |
Cascales E (2008). The type VI secretion toolkit. EMBO Rep, 9(8): 735–741
https://doi.org/10.1038/embor.2008.131
pmid: 18617888
|
25 |
Cascales E, Christie P J (2004). Agrobacterium VirB10, an ATP energy sensor required for type IV secretion. Proc Natl Acad Sci USA, 101(49): 17228–17233
https://doi.org/10.1073/pnas.0405843101
pmid: 15569944
|
26 |
Champion P A, Stanley S A, Champion M M, Brown E J, Cox J S (2006). C-terminal signal sequence promotes virulence factor secretion in Mycobacterium tuberculosis. Science, 313(5793): 1632–1636
https://doi.org/10.1126/science.1131167
pmid: 16973880
|
27 |
Christie P J, Atmakuri K, Krishnamoorthy V, Jakubowski S, Cascales E (2005). Biogenesis, architecture, and function of bacterial type IV secretion systems. Annu Rev Microbiol, 59(1): 451–485
https://doi.org/10.1146/annurev.micro.58.030603.123630
pmid: 16153176
|
28 |
Christie P J, Cascales E (2005). Structural and dynamic properties of bacterial type IV secretion systems. Mol Membr Biol, 22(1–2): 51–61
https://doi.org/10.1080/09687860500063316
pmid: 16092524
|
29 |
Cianciotto N P (2005). Type II secretion: a protein secretion system for all seasons. Trends Microbiol, 13(12): 581–588
https://doi.org/10.1016/j.tim.2005.09.005
pmid: 16216510
|
30 |
Cianciotto N P (2009). Many substrates and functions of type II secretion: lessons learned from Legionella pneumophila. Future Microbiol, 4(7): 797–805
https://doi.org/10.2217/fmb.09.53
pmid: 19722835
|
31 |
Coers J, Kagan J C, Matthews M, Nagai H, Zuckman D M, Roy C R (2000). Identification of Icm protein complexes that play distinct roles in the biogenesis of an organelle permissive for Legionella pneumophila intracellular growth. Mol Microbiol, 38(4): 719–736
https://doi.org/10.1046/j.1365-2958.2000.02176.x
pmid: 11115108
|
32 |
Converse S E, Cox J S (2005). A protein secretion pathway critical for Mycobacterium tuberculosis virulence is conserved and functional in Mycobacterium smegmatis. J Bacteriol, 187(4): 1238–1245
https://doi.org/10.1128/JB.187.4.1238-1245.2005
pmid: 15687187
|
33 |
Cornelis G R (2006). The type III secretion injectisome. Nat Rev Microbiol, 4(11): 811–825
https://doi.org/10.1038/nrmicro1526
pmid: 17041629
|
34 |
Coulthurst S J (2013). The Type VI secretion system - a widespread and versatile cell targeting system. Res Microbiol, 164(6): 640–654
https://doi.org/10.1016/j.resmic.2013.03.017
pmid: 23542428
|
35 |
Cover T L, Blanke S R (2005). Helicobacter pylori VacA, a paradigm for toxin multifunctionality. Nat Rev Microbiol, 3(4): 320–332
https://doi.org/10.1038/nrmicro1095
pmid: 15759043
|
36 |
d’Enfert C, Ryter A, Pugsley A P (1987). Cloning and expression in Escherichia coli of the Klebsiella pneumoniae genes for production, surface localization and secretion of the lipoprotein pullulanase. EMBO J, 6(11): 3531–3538
pmid: 3322811
|
37 |
Dai S, Zhou D (2004). Secretion and function of Salmonella SPI-2 effector SseF require its chaperone, SscB. J Bacteriol, 186(15): 5078–5086
https://doi.org/10.1128/JB.186.15.5078-5086.2004
pmid: 15262944
|
38 |
Daleke M H, Cascioferro A, de Punder K, Ummels R, Abdallah A M, van der Wel N, Peters P J, Luirink J, Manganelli R, Bitter W (2011). Conserved Pro-Glu (PE) and Pro-Pro-Glu (PPE) protein domains target LipY lipases of pathogenic mycobacteria to the cell surface via the ESX-5 pathway. J Biol Chem, 286(21): 19024–19034
https://doi.org/10.1074/jbc.M110.204966
pmid: 21471225
|
39 |
Daleke M H, van der Woude A D, Parret A H, Ummels R, de Groot A M, Watson D, Piersma S R, Jiménez C R, Luirink J, Bitter W, Houben E N (2012). Specific chaperones for the type VII protein secretion pathway. J Biol Chem, 287(38): 31939–31947
https://doi.org/10.1074/jbc.M112.397596
pmid: 22843727
|
40 |
De Buck E, H?per D, Lammertyn E, Hecker M, Anné J (2008). Differential 2-D protein gel electrophoresis analysis of Legionella pneumophila wild type and Tat secretion mutants. Int J Med Microbiol, 298(5–6): 449–461
https://doi.org/10.1016/j.ijmm.2007.06.003
pmid: 17723319
|
41 |
De Buck E, Lebeau I, Maes L, Geukens N, Meyen E, Van Mellaert L, Anné J, Lammertyn E (2004). A putative twin-arginine translocation pathway in Legionella pneumophila. Biochem Biophys Res Commun, 317(2): 654–661
https://doi.org/10.1016/j.bbrc.2004.03.091
pmid: 15063808
|
42 |
De Buck E, Maes L, Meyen E, Van Mellaert L, Geukens N, Anné J, Lammertyn E (2005). Legionella pneumophila Philadelphia-1 tatB and tatC affect intracellular replication and biofilm formation. Biochem Biophys Res Commun, 331(4): 1413–1420
https://doi.org/10.1016/j.bbrc.2005.04.060
pmid: 15883032
|
43 |
DebRoy S, Dao J, S?derberg M, Rossier O, Cianciotto N P (2006). Legionella pneumophilatype II secretome reveals unique exoproteins and a chitinase that promotes bacterial persistence in the lung. Proc Natl Acad Sci USA, 103(50): 19146–19151
https://doi.org/10.1073/pnas.0608279103
pmid: 17148602
|
44 |
Deiwick J, Nikolaus T, Shea J E, Gleeson C, Holden D W, Hensel M (1998). Mutations in Salmonella pathogenicity island 2 (SPI2) genes affecting transcription of SPI1 genes and resistance to antimicrobial agents. J Bacteriol, 180(18): 4775–4780
pmid: 9733677
|
45 |
Delepelaire P (2004). Type I secretion in gram-negative bacteria. Biochim Biophys Acta, 1694(1-3): 149–161
https://doi.org/10.1016/j.bbamcr.2004.05.001
pmid: 15546664
|
46 |
Duménil G, Isberg R R (2001). The Legionella pneumophila IcmR protein exhibits chaperone activity for IcmQ by preventing its participation in high-molecular-weight complexes. Mol Microbiol, 40(5): 1113–1127
https://doi.org/10.1046/j.1365-2958.2001.02454.x
pmid: 11401716
|
47 |
Figueira R, Holden D W (2012). Functions of the Salmonella pathogenicity island 2 (SPI-2) type III secretion system effectors. Microbiology, 158(Pt 5): 1147–1161
https://doi.org/10.1099/mic.0.058115-0
pmid: 22422755
|
48 |
Filloux A (2004). The underlying mechanisms of type II protein secretion. Biochim Biophys Acta, 1694(1-3): 163–179
https://doi.org/10.1016/j.bbamcr.2004.05.003
pmid: 15546665
|
49 |
Filloux A, Hachani A, Bleves S (2008). The bacterial type VI secretion machine: yet another player for protein transport across membranes. Microbiology, 154(Pt 6): 1570–1583
https://doi.org/10.1099/mic.0.2008/016840-0
pmid: 18524912
|
50 |
Fischetti V A (2008). Bacteriophage lysins as effective antibacterials. Curr Opin Microbiol, 11(5): 393–400
https://doi.org/10.1016/j.mib.2008.09.012
pmid: 18824123
|
51 |
Fritsch M J, Trunk K, Diniz J A, Guo M, Trost M, Coulthurst S J (2013). Proteomic identification of novel secreted antibacterial toxins of the Serratia marcescens type VI secretion system. Mol Cell Proteomics, 12(10): 2735–2749
https://doi.org/10.1074/mcp.M113.030502
pmid: 23842002
|
52 |
Galán J E (2001). Salmonella interactions with host cells: type III secretion at work. Annu Rev Cell Dev Biol, 17(1): 53–86
https://doi.org/10.1146/annurev.cellbio.17.1.53
pmid: 11687484
|
53 |
Galán J E, Wolf-Watz H (2006). Protein delivery into eukaryotic cells by type III secretion machines. Nature, 444(7119): 567–573
https://doi.org/10.1038/nature05272
pmid: 17136086
|
54 |
Garufi G, Butler E, Missiakas D (2008). ESAT-6-like protein secretion in Bacillus anthracis. J Bacteriol, 190(21): 7004–7011
https://doi.org/10.1128/JB.00458-08
pmid: 18723613
|
55 |
Gaspar A H, Machner M P (2014). VipD is a Rab5-activated phospholipase A1 that protects Legionella pneumophila from endosomal fusion. Proc Natl Acad Sci USA, 111(12): 4560–4565
https://doi.org/10.1073/pnas.1316376111
pmid: 24616501
|
56 |
Geukens N, De Buck E, Meyen E, Maes L, Vranckx L, Van Mellaert L, Anné J, Lammertyn E (2006). The type II signal peptidase of Legionella pneumophila. Res Microbiol, 157(9): 836–841
https://doi.org/10.1016/j.resmic.2006.06.003
pmid: 17005379
|
57 |
Guinn K M, Hickey M J, Mathur S K, Zakel K L, Grotzke J E, Lewinsohn D M, Smith S, Sherman D R (2004). Individual RD1-region genes are required for export of ESAT-6/CFP-10 and for virulence of Mycobacterium tuberculosis. Mol Microbiol, 51(2): 359–370
https://doi.org/10.1046/j.1365-2958.2003.03844.x
pmid: 14756778
|
58 |
Hales L M, Shuman H A (1999). Legionella pneumophilacontains a type II general secretion pathway required for growth in amoebae as well as for secretion of the Msp protease. Infect Immun, 67(7): 3662–3666
pmid: 10377156
|
59 |
Henderson I R, Nataro J P (2001). Virulence functions of autotransporter proteins. Infect Immun, 69(3): 1231–1243
https://doi.org/10.1128/IAI.69.3.1231-1243.2001
pmid: 11179284
|
60 |
Henderson I R, Navarro-Garcia F, Desvaux M, Fernandez R C, Ala’Aldeen D (2004). Type V protein secretion pathway: the autotransporter story. Microbiol Mol Biol Rev, 68(4): 692–744
https://doi.org/10.1128/MMBR.68.4.692-744.2004
pmid: 15590781
|
61 |
Higashide W, Zhou D (2006). The first 45 amino acids of SopA are necessary for InvB binding and SPI-1 secretion. J Bacteriol, 188(7): 2411–2420
https://doi.org/10.1128/JB.188.7.2411-2420.2006
pmid: 16547027
|
62 |
Holland I B, Schmitt L, Young J (2005). Type 1 protein secretion in bacteria, the ABC-transporter dependent pathway. Mol Membr Biol, 22(1-2): 29–39
https://doi.org/10.1080/09687860500042013
pmid: 16092522
|
63 |
Hood R D, Singh P, Hsu F, Güvener T, Carl M A, Trinidad R R, Silverman J M, Ohlson B B, Hicks K G, Plemel R L, Li M, Schwarz S, Wang W Y, Merz A J, Goodlett D R, Mougous J D (2010). A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe, 7(1): 25–37
https://doi.org/10.1016/j.chom.2009.12.007
pmid: 20114026
|
64 |
Houben E N, Bestebroer J, Ummels R, Wilson L, Piersma S R, Jiménez C R, Ottenhoff T H, Luirink J, Bitter W (2012). Composition of the type VII secretion system membrane complex. Mol Microbiol, 86(2): 472–484
https://doi.org/10.1111/j.1365-2958.2012.08206.x
pmid: 22925462
|
65 |
Hsu T, Hingley-Wilson S M, Chen B, Chen M, Dai A Z, Morin P M, Marks C B, Padiyar J, Goulding C, Gingery M, Eisenberg D, Russell R G, Derrick S C, Collins F M, Morris S L, King C H, Jacobs W R Jr (2003). The primary mechanism of attenuation of bacillus Calmette-Guerin is a loss of secreted lytic function required for invasion of lung interstitial tissue. Proc Natl Acad Sci USA, 100(21): 12420–12425
https://doi.org/10.1073/pnas.1635213100
pmid: 14557547
|
66 |
Hubber A, Roy C R (2010). Modulation of host cell function by Legionella pneumophila type IV effectors. Annu Rev Cell Dev Biol, 26(1): 261–283
https://doi.org/10.1146/annurev-cellbio-100109-104034
pmid: 20929312
|
67 |
Ilghari D, Lightbody K L, Veverka V, Waters L C, Muskett F W, Renshaw P S, Carr M D (2011). Solution structure of the Mycobacterium tuberculosis EsxG·EsxH complex: functional implications and comparisons with other M.tuberculosis Esx family complexes. J Biol Chem, 286(34): 29993–30002
https://doi.org/10.1074/jbc.M111.248732
pmid: 21730061
|
68 |
Ize B, Palmer T (2006). Microbiology. Mycobacteria’s export strategy. Science, 313(5793): 1583–1584
https://doi.org/10.1126/science.1132537
pmid: 16973866
|
69 |
Jacobi S, Heuner K (2003). Description of a putative type I secretion system in Legionella pneumophila. Int J Med Microbiol, 293(5): 349–358
https://doi.org/10.1078/1438-4221-00276
pmid: 14695063
|
70 |
Johnson T L, Abendroth J, Hol W G, Sandkvist M (2006). Type II secretion: from structure to function. FEMS Microbiol Lett, 255(2): 175–186
https://doi.org/10.1111/j.1574-6968.2006.00102.x
pmid: 16448494
|
71 |
Journet L, Hughes K T, Cornelis G R (2005). Type III secretion: a secretory pathway serving both motility and virulence. Mol Membr Biol, 22(1–2): 41–50
https://doi.org/10.1080/09687860500041858
pmid: 16092523
|
72 |
Kanamaru S (2009). Structural similarity of tailed phages and pathogenic bacterial secretion systems. Proc Natl Acad Sci USA, 106(11): 4067–4068
https://doi.org/10.1073/pnas.0901205106
pmid: 19276114
|
73 |
Komano T, Yoshida T, Narahara K, Furuya N (2000). The transfer region of IncI1 plasmid R64: similarities between R64 tra and legionella icm/dot genes. Mol Microbiol, 35(6): 1348–1359
https://doi.org/10.1046/j.1365-2958.2000.01769.x
pmid: 10760136
|
74 |
Koskiniemi S, Lamoureux J G, Nikolakakis K C, t’Kint de Roodenbeke C, Kaplan M D, Low D A, Hayes C S (2013). Rhs proteins from diverse bacteria mediate intercellular competition. Proc Natl Acad Sci USA, 110(17): 7032–7037
https://doi.org/10.1073/pnas.1300627110
pmid: 23572593
|
75 |
Lammertyn E, Anné J (2004). Protein secretion in Legionella pneumophila and its relation to virulence. FEMS Microbiol Lett, 238(2): 273–279
pmid: 15358411
|
76 |
Lammertyn E, Van Mellaert L, Meyen E, Lebeau I, De Buck E, Anné J, Geukens N (2004). Molecular and functional characterization of type I signal peptidase from Legionella pneumophila. Microbiology, 150(Pt 5): 1475–1483
https://doi.org/10.1099/mic.0.26973-0
pmid: 15133109
|
77 |
Leiman P G, Basler M, Ramagopal U A, Bonanno J B, Sauder J M, Pukatzki S, Burley S K, Almo S C, Mekalanos J J (2009). Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc Natl Acad Sci USA, 106(11): 4154–4159
https://doi.org/10.1073/pnas.0813360106
pmid: 19251641
|
78 |
Lewis K N, Liao R, Guinn K M, Hickey M J, Smith S, Behr M A, Sherman D R (2003). Deletion of RD1 from Mycobacterium tuberculosis mimics bacille Calmette-Guérin attenuation. J Infect Dis, 187(1): 117–123
https://doi.org/10.1086/345862
pmid: 12508154
|
79 |
Liles M R, Edelstein P H, Cianciotto N P (1999). The prepilin peptidase is required for protein secretion by and the virulence of the intracellular pathogen Legionella pneumophila. Mol Microbiol, 31(3): 959–970
https://doi.org/10.1046/j.1365-2958.1999.01239.x
pmid: 10048038
|
80 |
Lin J S, Ma L S, Lai E M (2013). Systematic dissection of the agrobacterium type VI secretion system reveals machinery and secreted components for subcomplex formation. PLoS ONE, 8(7): e67647
https://doi.org/10.1371/journal.pone.0067647
pmid: 23861778
|
81 |
Liu Y, Gao P, Banga S, Luo Z Q (2008). An in vivo gene deletion system for determining temporal requirement of bacterial virulence factors. Proc Natl Acad Sci USA, 105(27): 9385–9390
https://doi.org/10.1073/pnas.0801055105
pmid: 18599442
|
82 |
Liu Y, Luo Z Q (2007). The Legionella pneumophila effector SidJ is required for efficient recruitment of endoplasmic reticulum proteins to the bacterial phagosome. Infect Immun, 75(2): 592–603
https://doi.org/10.1128/IAI.01278-06
pmid: 17101649
|
83 |
Lossi N S, Dajani R, Freemont P, Filloux A (2011). Structure-function analysis of HsiF, a gp25-like component of the type VI secretion system, in Pseudomonas aeruginosa. Microbiology, 157(Pt 12): 3292–3305
https://doi.org/10.1099/mic.0.051987-0
pmid: 21873404
|
84 |
Luo Z Q, Isberg R R (2004). Multiple substrates of the Legionella pneumophila Dot/Icm system identified by interbacterial protein transfer. Proc Natl Acad Sci USA, 101(3): 841–846
https://doi.org/10.1073/pnas.0304916101
pmid: 14715899
|
85 |
Ma A T, McAuley S, Pukatzki S, Mekalanos J J (2009). Translocation of a Vibrio cholerae type VI secretion effector requires bacterial endocytosis by host cells. Cell Host Microbe, 5(3): 234–243
https://doi.org/10.1016/j.chom.2009.02.005
pmid: 19286133
|
86 |
Ma A T, Mekalanos J J (2010). In vivo actin cross-linking induced by Vibrio cholerae type VI secretion system is associated with intestinal inflammation. Proc Natl Acad Sci USA, 107(9): 4365–4370
https://doi.org/10.1073/pnas.0915156107
pmid: 20150509
|
87 |
Machner M P, Isberg R R (2006). Targeting of host Rab GTPase function by the intravacuolar pathogen Legionella pneumophila. Dev Cell, 11(1): 47–56
https://doi.org/10.1016/j.devcel.2006.05.013
pmid: 16824952
|
88 |
Mackman N, Holland I B (1984). Functional characterization of a cloned haemolysin determinant from E. coli of human origin, encoding information for the secretion of a 107K polypeptide. Mol Gen Genet, 196(1): 129–134
https://doi.org/10.1007/BF00334104
pmid: 6090863
|
89 |
Mahairas G G, Sabo P J, Hickey M J, Singh D C, Stover C K (1996). Molecular analysis of genetic differences between Mycobacterium bovis BCG and virulent M. bovis. J Bacteriol, 178(5): 1274–1282
pmid: 8631702
|
90 |
Marie C, Broughton W J, Deakin W J (2001). Rhizobium type III secretion systems: legume charmers or alarmers? Curr Opin Plant Biol, 4(4): 336–342
https://doi.org/10.1016/S1369-5266(00)00182-5
pmid: 11418344
|
91 |
Matthews M, Roy C R (2000). Identification and subcellular localization of the Legionella pneumophila IcmX protein: a factor essential for establishment of a replicative organelle in eukaryotic host cells. Infect Immun, 68(7): 3971–3982
https://doi.org/10.1128/IAI.68.7.3971-3982.2000
pmid: 10858211
|
92 |
Michiels T, Vanooteghem J C, Lambert de Rouvroit C, China B, Gustin A, Boudry P, Cornelis G R (1991). Analysis of virC, an operon involved in the secretion of Yop proteins by Yersinia enterocolitica. J Bacteriol, 173(16): 4994–5009
pmid: 1860816
|
93 |
Mougous J D, Cuff M E, Raunser S, Shen A, Zhou M, Gifford C A, Goodman A L, Joachimiak G, Ordo?ez C L, Lory S, Walz T, Joachimiak A, Mekalanos J J (2006). A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science, 312(5779): 1526–1530
https://doi.org/10.1126/science.1128393
pmid: 16763151
|
94 |
Murata T, Delprato A, Ingmundson A, Toomre D K, Lambright D G, Roy C R (2006). The Legionella pneumophila effector protein DrrA is a Rab1 guanine nucleotide-exchange factor. Nat Cell Biol, 8(9): 971–977
https://doi.org/10.1038/ncb1463
pmid: 16906144
|
95 |
Murdoch S L, Trunk K, English G, Fritsch M J, Pourkarimi E, Coulthurst S J (2011). The opportunistic pathogen Serratia marcescens utilizes type VI secretion to target bacterial competitors. J Bacteriol, 193(21): 6057–6069
https://doi.org/10.1128/JB.05671-11
pmid: 21890705
|
96 |
Nagai H, Kagan J C, Zhu X, Kahn R A, Roy C R (2002). A bacterial guanine nucleotide exchange factor activates ARF on Legionella phagosomes. Science, 295(5555): 679–682
https://doi.org/10.1126/science.1067025
pmid: 11809974
|
97 |
Nivaskumar M, Francetic O (2014). Type II secretion system: a magic beanstalk or a protein escalator. Biochim Biophys Acta, 1843(8): 1568–1577
https://doi.org/10.1016/j.bbamcr.2013.12.020
pmid: 24389250
|
98 |
Oomen C J, van Ulsen P, van Gelder P, Feijen M, Tommassen J, Gros P (2004). Structure of the translocator domain of a bacterial autotransporter. EMBO J, 23(6): 1257–1266
https://doi.org/10.1038/sj.emboj.7600148
pmid: 15014442
|
99 |
Page A L, Parsot C (2002). Chaperones of the type III secretion pathway: jacks of all trades. Mol Microbiol, 46(1): 1–11
https://doi.org/10.1046/j.1365-2958.2002.03138.x
pmid: 12366826
|
100 |
Pallen M J (2002). The ESAT-6/WXG100 superfamily — and a new Gram-positive secretion system? Trends Microbiol, 10(5): 209–212
https://doi.org/10.1016/S0966-842X(02)02345-4
pmid: 11973144
|
101 |
Poole S J, Diner E J, Aoki S K, Braaten B A, t’Kint de Roodenbeke C, Low D A, Hayes C S (2011). Identification of functional toxin/immunity genes linked to contact-dependent growth inhibition (CDI) and rearrangement hotspot (Rhs) systems. PLoS Genet, 7(8): e1002217
https://doi.org/10.1371/journal.pgen.1002217
pmid: 21829394
|
102 |
Pukatzki S, Ma A T, Revel A T, Sturtevant D, Mekalanos J J (2007). Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc Natl Acad Sci USA, 104(39): 15508–15513
https://doi.org/10.1073/pnas.0706532104
pmid: 17873062
|
103 |
Pukatzki S, Ma A T, Sturtevant D, Krastins B, Sarracino D, Nelson W C, Heidelberg J F, Mekalanos J J (2006). Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci USA, 103(5): 1528–1533
https://doi.org/10.1073/pnas.0510322103
pmid: 16432199
|
104 |
Pym A S, Brodin P, Brosch R, Huerre M, Cole S T (2002). Loss of RD1 contributed to the attenuation of the live tuberculosis vaccines Mycobacterium bovis BCG and Mycobacterium microti. Mol Microbiol, 46(3): 709–717
https://doi.org/10.1046/j.1365-2958.2002.03237.x
pmid: 12410828
|
105 |
Pym A S, Brodin P, Majlessi L, Brosch R, Demangel C, Williams A, Griffiths K E, Marchal G, Leclerc C, Cole S T (2003). Recombinant BCG exporting ESAT-6 confers enhanced protection against tuberculosis. Nat Med, 9(5): 533–539
https://doi.org/10.1038/nm859
pmid: 12692540
|
106 |
Ridenour D A, Cirillo S L, Feng S, Samrakandi M M, Cirillo J D (2003). Identification of a gene that affects the efficiency of host cell infection by Legionella pneumophila in a temperature-dependent fashion. Infect Immun, 71(11): 6256–6263
https://doi.org/10.1128/IAI.71.11.6256-6263.2003
pmid: 14573644
|
107 |
Robinson C G, Roy C R (2006). Attachment and fusion of endoplasmic reticulum with vacuoles containing Legionella pneumophila. Cell Microbiol, 8(5): 793–805
https://doi.org/10.1111/j.1462-5822.2005.00666.x
pmid: 16611228
|
108 |
Rodríguez-Escudero I, Ferrer N L, Rotger R, Cid V J, Molina M (2011). Interaction of the Salmonella typhimurium effector protein SopB with host cell Cdc42 is involved in intracellular replication. Mol Microbiol, 80(5): 1220–1240
https://doi.org/10.1111/j.1365-2958.2011.07639.x
pmid: 21435037
|
109 |
Rossier O, Cianciotto N P (2005). The Legionella pneumophila tatB gene facilitates secretion of phospholipase C, growth under iron-limiting conditions, and intracellular infection. Infect Immun, 73(4): 2020–2032
https://doi.org/10.1128/IAI.73.4.2020-2032.2005
pmid: 15784543
|
110 |
Rossier O, Dao J, Cianciotto N P (2008). The type II secretion system of Legionella pneumophila elaborates two aminopeptidases, as well as a metalloprotease that contributes to differential infection among protozoan hosts. Appl Environ Microbiol, 74(3): 753–761
https://doi.org/10.1128/AEM.01944-07
pmid: 18083880
|
111 |
Rossier O, Starkenburg S R, Cianciotto N P (2004). Legionella pneumophila type II protein secretion promotes virulence in the A/J mouse model of Legionnaires’ disease pneumonia. Infect Immun, 72(1): 310–321
https://doi.org/10.1128/IAI.72.1.310-321.2004
pmid: 14688110
|
112 |
Russell A B, LeRoux M, Hathazi K, Agnello D M, Ishikawa T, Wiggins P A, Wai S N, Mougous J D (2013). Diverse type VI secretion phospholipases are functionally plastic antibacterial effectors. Nature, 496(7446): 508–512
https://doi.org/10.1038/nature12074
pmid: 23552891
|
113 |
Russell A B, Singh P, Brittnacher M, Bui N K, Hood R D, Carl M A, Agnello D M, Schwarz S, Goodlett D R, Vollmer W, Mougous J D (2012). A widespread bacterial type VI secretion effector superfamily identified using a heuristic approach. Cell Host Microbe, 11(5): 538–549
https://doi.org/10.1016/j.chom.2012.04.007
pmid: 22607806
|
114 |
Sandkvist M (2001). Type II secretion and pathogenesis. Infect Immun, 69(6): 3523–3535
https://doi.org/10.1128/IAI.69.6.3523-3535.2001
pmid: 11349009
|
115 |
Sandkvist M, Michel L O, Hough L P, Morales V M, Bagdasarian M, Koomey M, DiRita V J, Bagdasarian M (1997). General secretion pathway (eps) genes required for toxin secretion and outer membrane biogenesis in Vibrio cholerae. J Bacteriol, 179(22): 6994–7003
pmid: 9371445
|
116 |
Segal G, Purcell M, Shuman H A (1998). Host cell killing and bacterial conjugation require overlapping sets of genes within a 22-kb region of the Legionella pneumophila genome. Proc Natl Acad Sci USA, 95(4): 1669–1674
https://doi.org/10.1073/pnas.95.4.1669
pmid: 9465074
|
117 |
Serra D O, Conover M S, Arnal L, Sloan G P, Rodriguez M E, Yantorno O M, Deora R (2011). FHA-mediated cell-substrate and cell-cell adhesions are critical for Bordetella pertussis biofilm formation on abiotic surfaces and in the mouse nose and the trachea. PLoS ONE, 6(12): e28811
https://doi.org/10.1371/journal.pone.0028811
pmid: 22216115
|
118 |
Sexton J A, Pinkner J S, Roth R, Heuser J E, Hultgren S J, Vogel J P (2004). The Legionella pneumophila PilT homologue DotB exhibits ATPase activity that is critical for intracellular growth. J Bacteriol, 186(6): 1658–1666
https://doi.org/10.1128/JB.186.6.1658-1666.2004
pmid: 14996796
|
119 |
Shen X, Banga S, Liu Y, Xu L, Gao P, Shamovsky I, Nudler E, Luo Z Q (2009). Targeting eEF1A by a Legionella pneumophila effector leads to inhibition of protein synthesis and induction of host stress response. Cell Microbiol, 11(6): 911–926
https://doi.org/10.1111/j.1462-5822.2009.01301.x
pmid: 19386084
|
120 |
Shneider M M, Buth S A, Ho B T, Basler M, Mekalanos J J, Leiman P G (2013). PAAR-repeat proteins sharpen and diversify the type VI secretion system spike. Nature, 500(7462): 350–353
https://doi.org/10.1038/nature12453
pmid: 23925114
|
121 |
Shrivastava R, Miller J F (2009). Virulence factor secretion and translocation by Bordetella species. Curr Opin Microbiol, 12(1): 88–93
https://doi.org/10.1016/j.mib.2009.01.001
pmid: 19186097
|
122 |
Silverman J M, Agnello D M, Zheng H, Andrews B T, Li M, Catalano C E, Gonen T, Mougous J D (2013). Haemolysin coregulated protein is an exported receptor and chaperone of type VI secretion substrates. Mol Cell, 51(5): 584–593
https://doi.org/10.1016/j.molcel.2013.07.025
pmid: 23954347
|
123 |
Silverman J M, Austin L S, Hsu F, Hicks K G, Hood R D, Mougous J D (2011). Separate inputs modulate phosphorylation-dependent and -independent type VI secretion activation. Mol Microbiol, 82(5): 1277–1290
https://doi.org/10.1111/j.1365-2958.2011.07889.x
pmid: 22017253
|
124 |
Silverman J M, Brunet Y R, Cascales E, Mougous J D (2012). Structure and regulation of the type VI secretion system. Annu Rev Microbiol, 66(1): 453–472
https://doi.org/10.1146/annurev-micro-121809-151619
pmid: 22746332
|
125 |
S?rensen A L, Nagai S, Houen G, Andersen P, Andersen A B (1995). Purification and characterization of a low-molecular-mass T-cell antigen secreted by Mycobacterium tuberculosis. Infect Immun, 63(5): 1710–1717
pmid: 7729876
|
126 |
Srikannathasan V, English G, Bui N K, Trunk K, O’Rourke P E, Rao V A, Vollmer W, Coulthurst S J, Hunter W N (2013). Structural basis for type VI secreted peptidoglycan DL-endopeptidase function, specificity and neutralization in Serratia marcescens. Acta Crystallogr D Biol Crystallogr, 69(Pt 12): 2468–2482
https://doi.org/10.1107/S0907444913022725
pmid: 24311588
|
127 |
St Geme J W 3rd, Yeo H J (2009). A prototype two-partner secretion pathway: the Haemophilus influenzae HMW1 and HMW2 adhesin systems. Trends Microbiol, 17(8): 355–360
https://doi.org/10.1016/j.tim.2009.06.002
pmid: 19660953
|
128 |
Stanley S A, Raghavan S, Hwang W W, Cox J S (2003). Acute infection and macrophage subversion by Mycobacterium tuberculosis require a specialized secretion system. Proc Natl Acad Sci USA, 100(22): 13001–13006
https://doi.org/10.1073/pnas.2235593100
pmid: 14557536
|
129 |
Stebbins C E, Galán J E (2001). Maintenance of an unfolded polypeptide by a cognate chaperone in bacterial type III secretion. Nature, 414(6859): 77–81
https://doi.org/10.1038/35102073
pmid: 11689946
|
130 |
Suarez G, Sierra J C, Erova T E, Sha J, Horneman A J, Chopra A K (2010). A type VI secretion system effector protein, VgrG1, from Aeromonas hydrophila that induces host cell toxicity by ADP ribosylation of actin. J Bacteriol, 192(1): 155–168
https://doi.org/10.1128/JB.01260-09
pmid: 19880608
|
131 |
Sun E W, Wagner M L, Maize A, Kemler D, Garland-Kuntz E, Xu L, Luo Z Q, Hollenbeck P J (2013). Legionella pneumophila infection of Drosophila S2 cells induces only minor changes in mitochondrial dynamics. PLoS ONE, 8(4): e62972
https://doi.org/10.1371/journal.pone.0062972
pmid: 23638172
|
132 |
Tauschek M, Gorrell R J, Strugnell R A, Robins-Browne R M (2002). Identification of a protein secretory pathway for the secretion of heat-labile enterotoxin by an enterotoxigenic strain of Escherichia coli. Proc Natl Acad Sci USA, 99(10): 7066–7071
https://doi.org/10.1073/pnas.092152899
pmid: 12011463
|
133 |
Thanassi D G, Stathopoulos C, Karkal A, Li H (2005). Protein secretion in the absence of ATP: the autotransporter, two-partner secretion and chaperone/usher pathways of gram-negative bacteria. Mol Membr Biol, 22(1–2): 63–72
https://doi.org/10.1080/09687860500063290
pmid: 16092525
|
134 |
Thomas S, Holland I B, Schmitt L (2013). The Type 1 secretion pathway - The hemolysin system and beyond. Biochim Biophys Acta, 1843(8): 1629–1641
pmid: 24129268
|
135 |
van Ulsen P, Rahman S U, Jong W S, Daleke-Schermerhorn M H, Luirink J (2013). Type V secretion: From biogenesis to biotechnology. Biochim Biophys Acta
pmid: 24269841
|
136 |
van Ulsen P, van Alphen L, ten Hove J, Fransen F, van der Ley P, Tommassen J (2003). A Neisserial autotransporter NalP modulating the processing of other autotransporters. Mol Microbiol, 50(3): 1017–1030
https://doi.org/10.1046/j.1365-2958.2003.03773.x
pmid: 14617158
|
137 |
Vincent C D, Friedman J R, Jeong K C, Buford E C, Miller J L, Vogel J P (2006). Identification of the core transmembrane complex of the Legionella Dot/Icm type IV secretion system. Mol Microbiol, 62(5): 1278–1291
https://doi.org/10.1111/j.1365-2958.2006.05446.x
pmid: 17040490
|
138 |
Vogel J P, Andrews H L, Wong S K, Isberg R R (1998). Conjugative transfer by the virulence system of Legionella pneumophila. Science, 279(5352): 873–876
https://doi.org/10.1126/science.279.5352.873
pmid: 9452389
|
139 |
Voulhoux R, Ball G, Ize B, Vasil M L, Lazdunski A, Wu L F, Filloux A (2001). Involvement of the twin-arginine translocation system in protein secretion via the type II pathway. EMBO J, 20(23): 6735–6741
https://doi.org/10.1093/emboj/20.23.6735
pmid: 11726509
|
140 |
Wagner J M, Evans T J, Korotkov K V (2014). Crystal structure of the N-terminal domain of EccA? ATPase from the ESX-1 secretion system of Mycobacterium tuberculosis. Proteins, 82(1): 159–163
https://doi.org/10.1002/prot.24351
pmid: 23818233
|
141 |
Welch R A, Dellinger E P, Minshew B, Falkow S (1981). Haemolysin contributes to virulence of extra-intestinal E. coli infections. Nature, 294(5842): 665–667
https://doi.org/10.1038/294665a0
pmid: 7031483
|
142 |
Wenren L M, Sullivan N L, Cardarelli L, Septer A N, Gibbs K A (2013). Two independent pathways for self-recognition in Proteus mirabilis are linked by type VI-dependent export. MBio, 4(4): 4
https://doi.org/10.1128/mBio.00374-13
pmid: 23882014
|
143 |
Whitney J C, Chou S, Russell A B, Biboy J, Gardiner T E, Ferrin M A, Brittnacher M, Vollmer W, Mougous J D (2013). Identification, structure, and function of a novel type VI secretion peptidoglycan glycoside hydrolase effector-immunity pair. J Biol Chem, 288(37): 26616–26624
https://doi.org/10.1074/jbc.M113.488320
pmid: 23878199
|
144 |
Wille T, Wagner C, Mittelst?dt W, Blank K, Sommer E, Malengo G, D?hler D, Lange A, Sourjik V, Hensel M, Gerlach R G (2014). SiiA and SiiB are novel type I secretion system subunits controlling SPI4-mediated adhesion of Salmonella enterica. Cell Microbiol, 16(2): 161–178
https://doi.org/10.1111/cmi.12222
pmid: 24119191
|
145 |
Xu L, Luo Z Q (2013). Cell biology of infection by Legionella pneumophila. Microbes Infect, 15(2): 157–167
https://doi.org/10.1016/j.micinf.2012.11.001
pmid: 23159466
|
146 |
Xu L, Shen X, Bryan A, Banga S, Swanson M S, Luo Z Q (2010). Inhibition of host vacuolar H+-ATPase activity by a Legionella pneumophila effector. PLoS Pathog, 6(3): e1000822
https://doi.org/10.1371/journal.ppat.1000822
pmid: 20333253
|
147 |
Zhang Y, Higashide W M, McCormick B A, Chen J, Zhou D (2006). The inflammation-associated Salmonella SopA is a HECT-like E3 ubiquitin ligase. Mol Microbiol, 62(3): 786–793
https://doi.org/10.1111/j.1365-2958.2006.05407.x
pmid: 17076670
|
148 |
Zheng J, Ho B, Mekalanos J J (2011). Genetic analysis of anti-amoebae and anti-bacterial activities of the type VI secretion system in Vibrio cholerae. PLoS ONE, 6(8): e23876
https://doi.org/10.1371/journal.pone.0023876
pmid: 21909372
|
149 |
Zheng J, Leung K Y (2007). Dissection of a type VI secretion system in Edwardsiella tarda. Mol Microbiol, 66(5): 1192–1206
https://doi.org/10.1111/j.1365-2958.2007.05993.x
pmid: 17986187
|
150 |
Zhou D, Mooseker M S, Galán J E (1999). Role of the S. typhimurium actin-binding protein SipA in bacterial internalization. Science, 283(5410): 2092–2095
https://doi.org/10.1126/science.283.5410.2092
pmid: 10092234
|
151 |
Zhou Y, Tao J, Yu H, Ni J, Zeng L, Teng Q, Kim K S, Zhao G P, Guo X, Yao Y (2012). Hcp family proteins secreted via the type VI secretion system coordinately regulate Escherichia coli K1 interaction with human brain microvascular endothelial cells. Infect Immun, 80(3): 1243–1251
https://doi.org/10.1128/IAI.05994-11
pmid: 22184413
|
152 |
Zhu W, Banga S, Tan Y, Zheng C, Stephenson R, Gately J, Luo Z Q (2011). Comprehensive identification of protein substrates of the Dot/Icm type IV transporter of Legionella pneumophila. PLoS ONE, 6(3): e17638
https://doi.org/10.1371/journal.pone.0017638
pmid: 21408005
|
153 |
Zhu W, Hammad L A, Hsu F, Mao Y, Luo Z Q (2013). Induction of caspase 3 activation by multiple Legionella pneumophila Dot/Icm substrates. Cell Microbiol, 15(11): 1783–1795
pmid: 23773455
|
154 |
Zusman T, Yerushalmi G, Segal G (2003). Functional similarities between the icm/dot pathogenesis systems of Coxiella burnetii and Legionella pneumophila. Infect Immun, 71: 3714–3723
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