Please wait a minute...
Frontiers in Biology

ISSN 1674-7984

ISSN 1674-7992(Online)

CN 11-5892/Q

Front. Biol.    2014, Vol. 9 Issue (6) : 437-447    https://doi.org/10.1007/s11515-014-1333-z
REVIEW
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
 Download: PDF(208 KB)   HTML
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
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.

Keywords bacterial pathogen      secretion system      virulence factors     
Corresponding Author(s): Li XU   
Just Accepted Date: 25 September 2014   Online First Date: 14 November 2014    Issue Date: 13 January 2015
 Cite this article:   
Li XU,Yancheng LIU. Protein secretion systems in bacterial pathogens[J]. Front. Biol., 2014, 9(6): 437-447.
 URL:  
https://academic.hep.com.cn/fib/EN/10.1007/s11515-014-1333-z
https://academic.hep.com.cn/fib/EN/Y2014/V9/I6/437
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
[1] Xin YANG, Fengyang DENG, Katrina M. RAMONELL. Receptor-like kinases and receptor-like proteins: keys to pathogen recognition and defense signaling in plant innate immunity[J]. Front Biol, 2012, 7(2): 155-166.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed