Received date: 31 May 2014
Accepted date: 15 Sep 2014
Published date: 13 Jan 2015
Copyright
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.
Key words： bacterial pathogen; secretion system; virulence factors
Li XU , Yancheng LIU . Protein secretion systems in bacterial pathogens[J]. Frontiers in Biology, 2014 , 9(6) : 437 -447 . DOI: 10.1007/s11515-014-1333-z
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 6 |
Backert S, Meyer T F (2006). Type IV secretion systems and their effectors in bacterial pathogenesis. Curr Opin Microbiol, 9(2): 207–217
|
| 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
|
| 8 |
Baptista C, Barreto H C, São-José C (2013). High levels of DegU-P activate an Esat-6-like secretion system in Bacillus subtilis. PLoS ONE, 8(7): e67840
|
| 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
|
| 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
|
| 11 |
Berks B C (1996). A common export pathway for proteins binding complex redox cofactors? Mol Microbiol, 22(3): 393–404
|
| 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
|
| 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
|
| 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
|
| 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
|
| 16 |
Bönemann 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
|
| 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
|
| 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
|
| 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
|
| 20 |
Burkinshaw B J, Strynadka N C (2014). Assembly and structure of the T3SS. Biochim Biophys Acta, 1843(8): 1649–1663
|
| 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
|
| 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
|
| 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
|
| 24 |
Cascales E (2008). The type VI secretion toolkit. EMBO Rep, 9(8): 735–741
|
| 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
|
| 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
|
| 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
|
| 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
|
| 29 |
Cianciotto N P (2005). Type II secretion: a protein secretion system for all seasons. Trends Microbiol, 13(12): 581–588
|
| 30 |
Cianciotto N P (2009). Many substrates and functions of type II secretion: lessons learned from Legionella pneumophila. Future Microbiol, 4(7): 797–805
|
| 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
|
| 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
|
| 33 |
Cornelis G R (2006). The type III secretion injectisome. Nat Rev Microbiol, 4(11): 811–825
|
| 34 |
Coulthurst S J (2013). The Type VI secretion system - a widespread and versatile cell targeting system. Res Microbiol, 164(6): 640–654
|
| 35 |
Cover T L, Blanke S R (2005). Helicobacter pylori VacA, a paradigm for toxin multifunctionality. Nat Rev Microbiol, 3(4): 320–332
|
| 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
|
| 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
|
| 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
|
| 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
|
| 40 |
De Buck E, Höper 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
|
| 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
|
| 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
|
| 43 |
DebRoy S, Dao J, Söderberg 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
|
| 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
|
| 45 |
Delepelaire P (2004). Type I secretion in gram-negative bacteria. Biochim Biophys Acta, 1694(1-3): 149–161
|
| 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
|
| 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
|
| 48 |
Filloux A (2004). The underlying mechanisms of type II protein secretion. Biochim Biophys Acta, 1694(1-3): 163–179
|
| 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
|
| 50 |
Fischetti V A (2008). Bacteriophage lysins as effective antibacterials. Curr Opin Microbiol, 11(5): 393–400
|
| 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
|
| 52 |
Galán J E (2001). Salmonella interactions with host cells: type III secretion at work. Annu Rev Cell Dev Biol, 17(1): 53–86
|
| 53 |
Galán J E, Wolf-Watz H (2006). Protein delivery into eukaryotic cells by type III secretion machines. Nature, 444(7119): 567–573
|
| 54 |
Garufi G, Butler E, Missiakas D (2008). ESAT-6-like protein secretion in Bacillus anthracis. J Bacteriol, 190(21): 7004–7011
|
| 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
|
| 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
|
| 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
|
| 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
|
| 59 |
Henderson I R, Nataro J P (2001). Virulence functions of autotransporter proteins. Infect Immun, 69(3): 1231–1243
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 68 |
Ize B, Palmer T (2006). Microbiology. Mycobacteria’s export strategy. Science, 313(5793): 1583–1584
|
| 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
|
| 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
|
| 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
|
| 72 |
Kanamaru S (2009). Structural similarity of tailed phages and pathogenic bacterial secretion systems. Proc Natl Acad Sci USA, 106(11): 4067–4068
|
| 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
|
| 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
|
| 75 |
Lammertyn E, Anné J (2004). Protein secretion in Legionella pneumophila and its relation to virulence. FEMS Microbiol Lett, 238(2): 273–279
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 93 |
Mougous J D, Cuff M E, Raunser S, Shen A, Zhou M, Gifford C A, Goodman A L, Joachimiak G, Ordoñez 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
|
| 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
|
| 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
|
| 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
|
| 97 |
Nivaskumar M, Francetic O (2014). Type II secretion system: a magic beanstalk or a protein escalator. Biochim Biophys Acta, 1843(8): 1568–1577
|
| 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
|
| 99 |
Page A L, Parsot C (2002). Chaperones of the type III secretion pathway: jacks of all trades. Mol Microbiol, 46(1): 1–11
|
| 100 |
Pallen M J (2002). The ESAT-6/WXG100 superfamily — and a new Gram-positive secretion system? Trends Microbiol, 10(5): 209–212
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 114 |
Sandkvist M (2001). Type II secretion and pathogenesis. Infect Immun, 69(6): 3523–3535
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 121 |
Shrivastava R, Miller J F (2009). Virulence factor secretion and translocation by Bordetella species. Curr Opin Microbiol, 12(1): 88–93
|
| 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
|
| 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
|
| 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
|
| 125 |
Sørensen 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
| 140 |
Wagner J M, Evans T J, Korotkov K V (2014). Crystal structure of the N-terminal domain of EccA₁ ATPase from the ESX-1 secretion system of Mycobacterium tuberculosis. Proteins, 82(1): 159–163
|
| 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
|
| 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
|
| 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
|
| 144 |
Wille T, Wagner C, Mittelstädt W, Blank K, Sommer E, Malengo G, Döhler 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
|
| 145 |
Xu L, Luo Z Q (2013). Cell biology of infection by Legionella pneumophila. Microbes Infect, 15(2): 157–167
|
| 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
|
| 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
|
| 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
|
| 149 |
Zheng J, Leung K Y (2007). Dissection of a type VI secretion system in Edwardsiella tarda. Mol Microbiol, 66(5): 1192–1206
|
| 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
|
| 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
|
| 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
|
| 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
|
| 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
|
/
| 〈 |
|
〉 |