Type V secretion: mechanism(s) of autotransport through the bacterial outer membrane

Leo, Jack C.; Grin, Iwan; Linke, Dirk

doi:10.1098/rstb.2011.0208

Cited by 269Bacterial Genetics and BiotechnologyEscherichia coli research studiesBacterial Infections and Vaccines

Type V secretion: mechanism(s) of autotransport through the bacterial outer membrane

Open access

Leo, Jack C., Grin, Iwan, Linke, Dirk·2012·Philosophical Transactions of the Royal Society B Biological Sciences

DOI 10.1098/rstb.2011.0208PMC PMC3297439

Open this paper in CoChat — free account

Abstract

Autotransport in Gram-negative bacteria denotes the ability of surface-localized proteins to cross the outer membrane (OM) autonomously. Autotransporters perform this task with the help of a β-barrel transmembrane domain localized in the OM. Different classes of autotransporters have been investigated in detail in recent years; classical monomeric but also trimeric autotransporters comprise many important bacterial virulence factors. So do the two-partner secretion systems, which are a special case as the transported protein resides on a different polypeptide chain than the transporter. Despite the great interest in these proteins, the exact mechanism of the transport process remains elusive. Moreover, different periplasmic and OM factors have been identified that play a role in the translocation, making the term 'autotransport' debatable. In this review, we compile the wealth of details known on the mechanism of single autotransporters from different classes and organisms, and put them into a bigger perspective. We also discuss recently discovered or rediscovered classes of autotransporters.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1098/rstb.2011.0208

Cites

123 of 123 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

The autotransporter family of Gram-negative bacteria is particularly rich in autoagglutinins.
“A class of proteins that is particularly rich in autoagglutinins is the autotransporter family of Gram-negative bacteria [66].”
From Bacterial autoaggregation (2018) · cites this paper as [66]
The Type Vc secretion section says trimeric autotransporters in Gram-negative pathogens are usually adhesins, but it does not say they cause bacterial autoagglutination. Searches for autoagglutinins, autoaggregation, and cell–cell adhesion found no passage establishing that the autotransporter family is particularly rich in autoagglutinins. The indexed copy provides no page number for these passages. (LLM, conf=0.72)
Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Curli biogenesis and function.
Barnhart, M. M., & Chapman, M. (2006) · Annual Review of Microbiology · doi:10.1146/annurev.micro.60.080805.142106 · Cited by 1,223 · see citing works
The Transporter Classification Database (TCDB): recent advances
Saier, M. H., Reddy, V. S., Tsu, B. V., Ahmed, M. S., Li, C., & Moreno‐Hagelsieb, G. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv1103 · Cited by 989 · see citing works
Type V Protein Secretion Pathway: the Autotransporter Story
Henderson, I. R., Navarro‐García, F., Desvaux, M., Fernandez, R. C., & Ala’Aldeen, D. A. A. (2004) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.68.4.692-744.2004 · Cited by 839 · see citing works
Type III Secretion Systems and Disease
Coburn, B. A., Sekirov, I., & Finlay, B. B. (2007) · Clinical Microbiology Reviews · doi:10.1128/cmr.00013-07 · Cited by 648 · see citing works
Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease
Pohlner, J., Halter, R., Beyreuther, K. T., & Meyer, T. F. (1987) · Nature · doi:10.1038/325458a0 · Cited by 635 · see citing works
Sec- and Tat-mediated protein secretion across the bacterial cytoplasmic membrane—Distinct translocases and mechanisms
Natale, P., Brüser, T., & Driessen, A. J. M. (2007) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2007.07.015 · Cited by 539 · see citing works
Carboxy-terminal phenylalanine is essential for the correct assembly of a bacterial outer membrane protein
Struyvé, M., Moons, M., & Tommassen, J. (1991) · Journal of Molecular Biology · doi:10.1016/0022-2836(91)90880-f · Cited by 481 · see citing works
The Transporter Classification Database: recent advances
Saier, M. H., Yen, M. R., Noto, K., Tamang, D. G., & Elkan, C. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn862 · Cited by 414 · see citing works
Type I secretion in gram-negative bacteria
Delepelaire, P. (2004) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2004.05.001 · Cited by 411 · see citing works
Gibbs motif sampling: Detection of bacterial outer membrane protein repeats
Neuwald, A. F., Liu, J. S., & Lawrence, C. E. (1995) · Protein Science · doi:10.1002/pro.5560040820 · Cited by 392 · see citing works
Structural basis for the regulated protease and chaperone function of DegP
Krojer, T. J., Sawa-Makarska, J. Z., Schäfer, E., Saibil, H. R., Ehrmann, M., & Clausen, T. (2008) · Nature · doi:10.1038/nature07004 · Cited by 368 · see citing works
Structure of the translocator domain of a bacterial autotransporter
Oomen, C. J., van Ulsen, P., Gelder, P. V., et al. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600148 · Cited by 363 · see citing works
Structure and sequence analysis of Yersinia YadA and Moraxella UspAs reveal a novel class of adhesins
Hoiczyk, E., Roggenkamp, A., Reichenbecher, M., Lupas, A., & Heesemann, J. (2000) · The EMBO Journal · doi:10.1093/emboj/19.22.5989 · Cited by 359 · see citing works
Membrane protein architects: the role of the BAM complex in outer membrane protein assembly
Knowles, T. J., Scott-Tucker, A., Overduin, M., & Henderson, I. R. (2009) · Nature Reviews Microbiology · doi:10.1038/nrmicro2069 · Cited by 352 · see citing works
The Bacterial Twin-Arginine Translocation Pathway
Lee, P. A., Tullman‐Ercek, D., & Georgiou, G. (2006) · Annual Review of Microbiology · doi:10.1146/annurev.micro.60.080805.142212 · Cited by 348 · see citing works
Secretion and subcellular localizations of bacterial proteins: a semantic awareness issue
Desvaux, M., Hébraud, M., Talon, R., & Henderson, I. R. (2009) · Trends in Microbiology · doi:10.1016/j.tim.2009.01.004 · Cited by 347 · see citing works
Type IV secretion systems: versatility and diversity in function
Walldén, K., Rivera-Calzada, Á., & Waksman, G. (2010) · Cellular Microbiology · doi:10.1111/j.1462-5822.2010.01499.x · Cited by 345 · see citing works
Assembly Factor Omp85 Recognizes Its Outer Membrane Protein Substrates by a Species-Specific C-Terminal Motif
Robert, V., Volokhina, E. B., Senf, F., et al. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040377 · Cited by 327 · see citing works
β-Barrel Membrane Protein Assembly by the Bam Complex
Hagan, C. L., Silhavy, T. J., & Kahne, D. E. (2011) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-061408-144611 · Cited by 315 · see citing works
Trimeric autotransporter adhesins: variable structure, common function
Linke, D., Riess, T. M., Autenrieth, I. B., Lupas, A. N., & Kempf, V. A. J. (2006) · Trends in Microbiology · doi:10.1016/j.tim.2006.04.005 · Cited by 308 · see citing works
Self-citation
Pertactin, an Arg-Gly-Asp-containing Bordetella pertussis surface protein that promotes adherence of mammalian cells.
Leininger, E. C., Roberts, M., KENIMER, J. G., Charles, I. G., Fairweather, N., Novotný, P., & Brennan, M. J. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.2.345 · Cited by 295 · see citing works
The Sec protein-translocation pathway
Mori, H., & Ito, K. (2001) · Trends in Microbiology · doi:10.1016/s0966-842x(01)02174-6 · Cited by 285 · see citing works
Two‐partner secretion in Gram‐negative bacteria: a thrifty, specific pathway for large virulence proteins
Jacob‐Dubuisson, F., Locht, C., & Antoine, R. (2001) · Molecular Microbiology · doi:10.1046/j.1365-2958.2001.02278.x · Cited by 261 · see citing works
Structure of the Membrane Protein FhaC: A Member of the Omp85-TpsB Transporter Superfamily
Clantin, B., Delattre, A., Rucktooa, P., et al. (2007) · Science · doi:10.1126/science.1143860 · Cited by 256 · see citing works
ESX/type VII secretion systems and their role in host–pathogen interaction
Siméone, R., Bottai, D., & Brosch, R. (2009) · Current Opinion in Microbiology · doi:10.1016/j.mib.2008.11.003 · Cited by 250 · see citing works
Type II secretion: from structure to function
Johnson, T. L., Abendroth, J. A., Hol, W. G. J., et al. (2006) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2006.00102.x · Cited by 247 · see citing works
Cloning and expression of an adhesin (AIDA-I) involved in diffuse adherence of enteropathogenic Escherichia coli
Benz, I., & Schmidt, M. (1989) · Infection and Immunity · doi:10.1128/iai.57.5.1506-1511.1989 · Cited by 238 · see citing works
The Autodisplay Story, from Discovery to Biotechnical and Biomedical Applications
Jose, J., & Meyer, T. F. (2007) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00011-07 · Cited by 231 · see citing works
Protein targeting by the bacterial twin-arginine translocation (Tat) pathway
Berks, B. C., Palmer, T., & Sargent, F. (2005) · Current Opinion in Microbiology · doi:10.1016/j.mib.2005.02.010 · Cited by 227 · see citing works
Bartonella Adhesin A Mediates a Proangiogenic Host Cell Response
Riess, T. M., Andersson, S. G. E., Lupas, A. N., Schaller, M., Schäfer, A., Kyme, P. A., Martin, J., Wälzlein, J.-H., Ehehalt, U., Lindroos, H. L., et al. (2004) · The Journal of Experimental Medicine · doi:10.1084/jem.20040500 · Cited by 224 · see citing works
Autodisplay: one-component system for efficient surface display and release of soluble recombinant proteins from Escherichia coli
Maurer, J., Jose, J., & Meyer, T. F. (1997) · Journal of Bacteriology · doi:10.1128/jb.179.3.794-804.1997 · Cited by 217 · see citing works
Isolation and characterization of a gene involved in hemagglutination by an avian pathogenic Escherichia coli strain
Provence, D. L., & Curtiss, R. (1994) · Infection and Immunity · doi:10.1128/iai.62.4.1369-1380.1994 · Cited by 217 · see citing works
The Yersinia adhesin YadA collagen‐binding domain structure is a novel left‐handed parallel β‐roll
Nummelin, H., Merckel, M. C., Leo, J. C., Lankinen, H., Skurnik, M., & Goldman, A. (2004) · EMBO Journal · doi:10.1038/sj.emboj.7600100 · Cited by 214 · see citing works
Self-citation
Molecular Analysis of Transport and Oligomerization of the Yersinia enterocolitica Adhesin YadA
Roggenkamp, A., Ackermann, N., Jacobi, C. A., Trülzsch, K., Hoffmann, H., & Heesemann, J. (2003) · Journal of Bacteriology · doi:10.1128/jb.185.13.3735-3744.2003 · Cited by 209 · see citing works
Pertactin β-helix folding mechanism suggests common themes for the secretion and folding of autotransporter proteins
Junker, M., Schuster, C. C., McDonnell, A. V., Sorg, K. A., Finn, M. C., Berger, B., & Clark, P. L. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0507923103 · Cited by 208 · see citing works
The crystal structure of filamentous hemagglutinin secretion domain and its implications for the two-partner secretion pathway
Clantin, B., Hodak, H., Willery, E., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0400291101 · Cited by 189 · see citing works
Interaction of an autotransporter passenger domain with BamA during its translocation across the bacterial outer membrane
Ieva, R., & Bernstein, H. D. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0907912106 · Cited by 186 · see citing works
Crystal structure of the FimD usher bound to its cognate FimC–FimH substrate
Phan, G., Remaut, H. K., Wang, T., Allen, W. J., Pirker, K. F., Lebedev, A. A., Henderson, N. S., Geibel, S., Volkan, E., Yan, J., et al. (2011) · Nature · doi:10.1038/nature10109 · Cited by 185 · see citing works
Biogenesis of β-barrel membrane proteins in bacteria and eukaryotes: evolutionary conservation and divergence
Walther, D. M., Rapaport, D., & Tommassen, J. (2009) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-009-0029-z · Cited by 174 · see citing works
Structure of the outer membrane translocator domain of the Haemophilus influenzae Hia trimeric autotransporter
Meng, G., Surana, N. K., Geme, J. W. S., & Waksman, G. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601132 · Cited by 171 · see citing works
Beta‐helix model for the filamentous haemagglutinin adhesin of Bordetella pertussis and related bacterial secretory proteins
Kajava, A. V., Cheng, N., Cleaver, R., Kessel, M., Simon, M. N., Willery, E., Jacob‐Dubuisson, F., Locht, C., & Steven, A. C. (2001) · Molecular Microbiology · doi:10.1046/j.1365-2958.2001.02598.x · Cited by 169 · see citing works
Autotransporter structure reveals intra-barrel cleavage followed by conformational changes
Barnard, T. J., Dautin, N., Lukacik, P., et al. (2007) · Nature Structural & Molecular Biology · doi:10.1038/nsmb1322 · Cited by 165 · see citing works
Common structural features of IgA1 protease‐like outer membrane protein autotransporters
Jose, J., Jähnig, F., & Meyer, T. F. (1995) · Molecular Microbiology · doi:10.1111/j.1365-2958.1995.mmi_18020378.x · Cited by 161 · see citing works
Crystal Structure of a Full-Length Autotransporter
van den Berg, B. (2010) · Journal of Molecular Biology · doi:10.1016/j.jmb.2009.12.061 · Cited by 161 · see citing works
IgA Protease Production as a Characteristic Distinguishing Pathogenic from Harmless Neisseriaceae
Mulks, M. H., & Plaut, A. G. (1978) · New England Journal of Medicine · doi:10.1056/nejm197811022991802 · Cited by 154 · see citing works
Subtilisin‐like autotransporter serves as maturation protease in a bacterial secretion pathway
Coutte, L., Antoine, R., Drobecq, H., Locht, C., & Jacob‐Dubuisson, F. (2001) · The EMBO Journal · doi:10.1093/emboj/20.18.5040 · Cited by 152 · see citing works
Tubules and donuts: a type VI secretion story
Bönemann, G., Pietrosiuk, A., & Mogk, A. (2010) · Molecular Microbiology · doi:10.1111/j.1365-2958.2010.07171.x · Cited by 146 · see citing works
Sequential and spatially restricted interactions of assembly factors with an autotransporter β domain
Ieva, R., Tian, P., Peterson, J. H., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1103827108 · Cited by 145 · see citing works
An unusual signal peptide facilitates late steps in the biogenesis of a bacterial autotransporter
Szabady, R. L., Peterson, J. H., Skillman, K. M., & Bernstein, H. D. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0406055102 · Cited by 137 · see citing works
The Bam (Omp85) complex is involved in secretion of the autotransporter haemoglobin protease
Saurı́, A., Soprova, Z., Wickström, D., Gier, J. D., van der Schors, R. C., Smit, A. B., Jong, W. S. P., & Luirink, J. (2009) · Microbiology · doi:10.1099/mic.0.034991-0 · Cited by 135 · see citing works
Vectorial transport and folding of an autotransporter virulence protein during outer membrane secretion
Junker, M., Besingi, R. N., & Clark, P. L. (2009) · Molecular Microbiology · doi:10.1111/j.1365-2958.2009.06607.x · Cited by 135 · see citing works
Structural basis for recognition of the translocated intimin receptor (Tir) by intimin from enteropathogenic Escherichia coli
Batchelor, M. J., Prasannan, S., Daniell, S. J., Reece, S. T., Connerton, I. F., Bloomberg, G. B., Gordon Dougan, B., Frankel, G. M., & Matthews, S. (2000) · The EMBO Journal · doi:10.1093/emboj/19.11.2452 · Cited by 131 · see citing works
Signal Recognition Particle (SRP)-mediated Targeting and Sec-dependent Translocation of an Extracellular Escherichia coli Protein*
Sijbrandi, R., Urbanus, M., ten Hagen-Jongman, C. T., Bernstein, H., Oudega, B., Otto, B., & Luirink, J. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m211630200 · Cited by 130 · see citing works
Roles of Periplasmic Chaperone Proteins in the Biogenesis of Serine Protease Autotransporters of Enterobacteriaceae
Ruı́z-Pérez, F., Henderson, I. R., Leyton, D. L., Rossiter, A. E., Zhang, Y., & Nataro, J. P. (2009) · Journal of Bacteriology · doi:10.1128/jb.00754-09 · Cited by 129 · see citing works
Signaling and invasin-promoted uptake via integrin receptors
Isberg, R. R., Hamburger, Z. A., & Dersch, P. (2000) · Microbes and Infection · doi:10.1016/s1286-4579(00)90364-2 · Cited by 122 · see citing works
Requirement for YaeT in the Outer Membrane Assembly of Autotransporter Proteins
Jain, S., & Goldberg, M. B. (2007) · Journal of Bacteriology · doi:10.1128/jb.00228-07 · Cited by 115 · see citing works
The Haemophilus influenzae Hia Adhesin Is an Autotransporter Protein That Remains Uncleaved at the C Terminus and Fully Cell Associated
Geme, J. W. S., & Cutter, D. (2000) · Journal of Bacteriology · doi:10.1128/jb.182.21.6005-6013.2000 · Cited by 111 · see citing works
Intimin and the host cell — is it bound to end in Tir(s)?
Frankel, G. (2001) · Trends in Microbiology · doi:10.1016/s0966-842x(01)02016-9 · Cited by 110 · see citing works
Protein secretion in the absence of ATP: the autotransporter, two-partner secretion and chaperone/usher pathways of Gram-negative bacteria (Review)
Thanassi, D. G., Stathopoulos, C., Karkal, A., & Li, H. (2005) · Molecular Membrane Biology · doi:10.1080/09687860500063290 · Cited by 101 · see citing works
The secretion pathway of IgA protease‐type proteins in gram‐negative bacteria
Klauser, T., Pohlner, J. E., & Meyer, T. F. (1993) · BioEssays · doi:10.1002/bies.950151205 · Cited by 101 · see citing works
Secretion of a bacterial virulence factor is driven by the folding of a C-terminal segment
Peterson, J. H., Tian, P., Ieva, R., Dautin, N., & Bernstein, H. D. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1009491107 · Cited by 101 · see citing works
Absence of periplasmic DsbA oxidoreductase facilitates export of cysteine-containing passenger proteins to the Escherichia coli cell surface via the Igaβ autotransporter pathway
Jose, J., Krämer, J., Klauser, T., et al. (1996) · Gene · doi:10.1016/0378-1119(96)00343-5 · Cited by 100 · see citing works
Domain annotation of trimeric autotransporter adhesins—daTAA
Szczęsny, P., & Lupas, A. N. (2008) · Bioinformatics · doi:10.1093/bioinformatics/btn118 · Cited by 100 · see citing works
Secretion signal of the filamentous haemagglutinin, a model two‐partner secretion substrate
Hodak, H., Clantin, B., Willery, E., et al. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2006.05242.x · Cited by 98 · see citing works
The Pseudomonas aeruginosa patatin‐like protein PlpD is the archetype of a novel Type V secretion system
Salacha, R., Kovačić, F., Brochier‐Armanet, C., et al. (2010) · Environmental Microbiology · doi:10.1111/j.1462-2920.2010.02174.x · Cited by 97 · see citing works
Topology and maturation of filamentous haemagglutinin suggest a new model for two‐partner secretion
Mazar, J., & Cotter, P. A. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2006.05392.x · Cited by 97 · see citing works
Mutational analysis of the Bordetella pertussis fim/fha gene cluster: identification of a gene with sequence similarities to haemolysin accessory genes involved in export of FHA
Willems, R. J. L., Geuijen, C. A. W., van der Heide, H. G. J., et al. (1994) · Molecular Microbiology · doi:10.1111/j.1365-2958.1994.tb00314.x · Cited by 97 · see citing works
HHomp—prediction and classification of outer membrane proteins
Remmert, M., Linke, D., Lupas, A. N., & Söding, J. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp325 · Cited by 96 · see citing works
Self-citation
Evolution of Outer Membrane β-Barrels from an Ancestral ββ Hairpin
Remmert, M., Biegert, A., Linke, D., Lupas, A. N., & Söding, J. (2010) · Molecular Biology and Evolution · doi:10.1093/molbev/msq017 · Cited by 96 · see citing works
Self-citation
Incorporation of a polypeptide segment into the β‐domain pore during the assembly of a bacterial autotransporter
Ieva, R., Skillman, K. M., & Bernstein, H. D. (2007) · Molecular Microbiology · doi:10.1111/j.1365-2958.2007.06048.x · Cited by 93 · see citing works
Studying membrane proteins through the eyes of the genetic code revealed a strong uracil bias in their coding mRNAs
Prilusky, J., & Bibi, E. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0902029106 · Cited by 91 · see citing works
Folding kinetics of the outer membrane proteins OmpA and FomA into phospholipid bilayers
Kleinschmidt, J. H. (2006) · Chemistry and Physics of Lipids · doi:10.1016/j.chemphyslip.2006.02.004 · Cited by 90 · see citing works
Gene Duplication of the Eight-stranded β-Barrel OmpX Produces a Functional Pore: A Scenario for the Evolution of Transmembrane β-Barrels
Arnold, T., Graewert, M. A., Nußberger, S., Lupas, A. N., & Linke, D. (2006) · Journal of Molecular Biology · doi:10.1016/j.jmb.2006.12.029 · Cited by 85 · see citing works
Self-citation
Structure of the Head of the Bartonella Adhesin BadA
Szczęsny, P., Linke, D., Ursinus, A., Bär, K., Schwarz, H., Riess, T. M., Kempf, V. A. J., Lupas, A. N., Martin, J., & Zeth, K. (2008) · PLoS Pathogens · doi:10.1371/journal.ppat.1000119 · Cited by 84 · see citing works
Self-citation
The Moraxella adhesin UspA1 binds to its human CEACAM1 receptor by a deformable trimeric coiled‐coil
Conners, R., Hill, D. J., Borodina, E. V., Agnew, C., Daniell, S. J., Burton, N. M., Sessions, R. B., Clarke, A. R., Catto, L. E., Lammie, D., et al. (2008) · The EMBO Journal · doi:10.1038/emboj.2008.101 · Cited by 83 · see citing works
Maturation and secretion of the non‐typable Haemophilus influenzae HMW1 adhesin: roles of the N‐terminal and C‐terminal domains
Grass, S. A., & Geme, J. W. S. (2000) · Molecular Microbiology · doi:10.1046/j.1365-2958.2000.01812.x · Cited by 82 · see citing works
C-terminal amino acid residues of the trimeric autotransporter adhesin YadA of Yersinia enterocolitica are decisive for its recognition and assembly by BamA
Lehr, U., Schütz, M. S., Oberhettinger, P., et al. (2010) · Molecular Microbiology · doi:10.1111/j.1365-2958.2010.07377.x · Cited by 80 · see citing works
Low Cyst(e)ine Content of Bacterial Extracellular Proteins: Its Possible Physiological Significance
Pollock, M. R., & Richmond, M. H. (1962) · Nature · doi:10.1038/194446a0 · Cited by 79 · see citing works
Role of Periplasmic Chaperones and BamA (YaeT/Omp85) in Folding and Secretion of Intimin from EnteropathogenicEscherichia coliStrains
Bodelón, G., Marín, E., & Fernández, L. Á. (2009) · Journal of Bacteriology · doi:10.1128/jb.00458-09 · Cited by 79 · see citing works
New insight into the molecular mechanisms of two-partner secretion
Mazar, J., & Cotter, P. A. (2007) · Trends in Microbiology · doi:10.1016/j.tim.2007.10.005 · Cited by 78 · see citing works
A coiled-coil motif that sequesters ions to the hydrophobic core
Hartmann, M. D., Ridderbusch, O., Zeth, K., Albrecht, R., Testa, O. D., Woolfson, D. N., Sauer, G., Dunin-Horkawicz, S., Lupas, A. N., & Alvarez, B. H. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0907256106 · Cited by 78 · see citing works
Self‐association of EPEC intimin mediated by the β‐barrel‐containing anchor domain: a role in clustering of the Tir receptor
Touzé, T., Hayward, R. D., Eswaran, J., et al. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03830.x · Cited by 77 · see citing works
The Tir‐binding region of enterohaemorrhagic Escherichia coli intimin is sufficient to trigger actin condensation after bacterial‐induced host cell signalling
Liu, H., Magoun, L., Luperchio, S. A., et al. (1999) · Molecular Microbiology · doi:10.1046/j.1365-2958.1999.01574.x · Cited by 77 · see citing works
Lack of functional complementation between Bordetella pertussis filamentous hemagglutinin and Proteus mirabilis HpmA hemolysin secretion machineries
Jacob‐Dubuisson, F., Buisine, C., Willery, E., et al. (1997) · Journal of Bacteriology · doi:10.1128/jb.179.3.775-783.1997 · Cited by 76 · see citing works
A Conserved Glycine Residue of Trimeric Autotransporter Domains Plays a Key Role inYersiniaAdhesin A Autotransport
Grosskinsky, U., Schütz, M. S., Fritz, M., Schmid, Y., Lamparter, M. C., Szczęsny, P., Lupas, A. N., Autenrieth, I. B., & Linke, D. (2007) · Journal of Bacteriology · doi:10.1128/jb.00985-07 · Cited by 76 · see citing works
Self-citation
Display of Passenger Proteins on the Surface ofEscherichia coliK-12 by the EnterohemorrhagicE. coliIntimin EaeA
Wentzel, A., Christmann, A., Adams, T., et al. (2001) · Journal of Bacteriology · doi:10.1128/jb.183.24.7273-7284.2001 · Cited by 72 · see citing works
The Structure of the Haemophilus influenzae HMW1 Pro-piece Reveals a Structural Domain Essential for Bacterial Two-partner Secretion
Yeo, H., Yokoyama, T., Walkiewicz, K. W., et al. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m705750200 · Cited by 71 · see citing works
Common themes and variations in serine protease autotransporters
Yen, Y. T., Kostakioti, M., Henderson, I. R., & Stathopoulos, C. (2008) · Trends in Microbiology · doi:10.1016/j.tim.2008.05.003 · Cited by 69 · see citing works
Evidence that a globular conformation is not compatible with FhaC‐mediated secretion of the Bordetella pertussis filamentous haemagglutinin
Guédin, S., Willery, E., Locht, C., et al. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.00970.x · Cited by 69 · see citing works
Identification of Secretion Determinants of the Bordetella pertussis BrkA Autotransporter
Oliver, D. C., Huang, G. H., & Fernandez, R. C. (2003) · Journal of Bacteriology · doi:10.1128/jb.185.2.489-495.2003 · Cited by 69 · see citing works
N‐terminal characterization of the Bordetella pertussis filamentous haemagglutinin
Lambert‐Buisine, C., Willery, E., Locht, C., et al. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.00892.x · Cited by 68 · see citing works
Omp85 from the Thermophilic Cyanobacterium Thermosynechococcus elongatus Differs from Proteobacterial Omp85 in Structure and Domain Composition
Arnold, T., Zeth, K., & Linke, D. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.112516 · Cited by 67 · see citing works
Self-citation
The Structure of E. coli IgG-Binding Protein D Suggests a General Model for Bending and Binding in Trimeric Autotransporter Adhesins
Leo, J. C., Łyskowski, A., Hattula, K., Hartmann, M. D., Schwarz, H., Butcher, S. J., Linke, D., Lupas, A. N., & Goldman, A. (2011) · Structure · doi:10.1016/j.str.2011.03.021 · Cited by 67 · see citing works
Self-citation
Two-step and one-step secretion mechanisms in Gram-negative bacteria: contrasting the type IV secretion system and the chaperone-usher pathway of pilus biogenesis
Rêgo, A. T., Chandran, V., & Waksman, G. (2010) · Biochemical Journal · doi:10.1042/bj20091518 · Cited by 65 · see citing works
Intimin and Invasin Export Their C-Terminus to the Bacterial Cell Surface Using an Inverse Mechanism Compared to Classical Autotransport
Oberhettinger, P., Schütz, M. S., Leo, J. C., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0047069 · Cited by 63 · see citing works
Self-citation
The Bacterial Intimins and Invasins: A Large and Novel Family of Secreted Proteins
Tsai, J. C., Yen, M., Castillo, R., Leyton, D. L., Henderson, I. R., & Saier, M. H. (2010) · PLoS ONE · doi:10.1371/journal.pone.0014403 · Cited by 61 · see citing works
Substrate recognition by the POTRA domains of TpsB transporter FhaC
Delattre, A., Saint, N., Clantin, B., Willery, E., Lippens, G. M., Locht, C., Villeret, V., & Jacob‐Dubuisson, F. (2011) · Molecular Microbiology · doi:10.1111/j.1365-2958.2011.07680.x · Cited by 59 · see citing works
Purification of the YadA membrane anchor for secondary structure analysis and crystallization
Wollmann, P., Zeth, K., Lupas, A. N., & Linke, D. (2006) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2005.11.009 · Cited by 58 · see citing works
Self-citation
A Conserved Aromatic Residue in the Autochaperone Domain of the Autotransporter Hbp Is Critical for Initiation of Outer Membrane Translocation
Soprova, Z., Saurı́, A., van Ulsen, P., et al. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.180505 · Cited by 58 · see citing works
Interaction of FkpA, a peptidyl-prolylcis/transisomerase with EspP autotransporter protein
Ruı́z-Pérez, F., Henderson, I. R., & Nataro, J. P. (2010) · Gut Microbes · doi:10.4161/gmic.1.5.13436 · Cited by 53 · see citing works
Architecture and Adhesive Activity of the Haemophilus influenzae Hsf Adhesin
Cotter, S. E., Yeo, H., Juehne, T. I., et al. (2005) · Journal of Bacteriology · doi:10.1128/jb.187.13.4656-4664.2005 · Cited by 52 · see citing works
A prototype two-partner secretion pathway: the Haemophilus influenzae HMW1 and HMW2 adhesin systems
Geme, J. W. S., & Yeo, H. (2009) · Trends in Microbiology · doi:10.1016/j.tim.2009.06.002 · Cited by 51 · see citing works
Renaming protein secretion in the Gram-negative bacteria
Henderson, I. R., Nataro, J. P., Kaper, J. B., Meyer, T. F., Farrand, S. K., Burns, D., Finlay, B. B., & Geme, J. W. S. (2000) · Trends in Microbiology · doi:10.1016/s0966-842x(00)01814-x · Cited by 48 · see citing works
Biogenesis of bacterial inner-membrane proteins
Facey, S. J., & Kühn, A. (2010) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-010-0303-0 · Cited by 48 · see citing works
Role of DegP for two‐partner secretion in Bordetella
Baud, C., Hodak, H., Willery, E., Drobecq, H., Locht, C., Jamin, M., & Jacob‐Dubuisson, F. (2009) · Molecular Microbiology · doi:10.1111/j.1365-2958.2009.06860.x · Cited by 47 · see citing works
Activation and Secretion of Serratia Hemolysin
Braun, V., Ondraczek, R., & Hobbie, S. (1993) · Zentralblatt für Bakteriologie · doi:10.1016/s0934-8840(11)80847-9 · Cited by 45 · see citing works
Autotransporter and Two-Partner Secretion: Delivery of Large-Size Virulence Factors by Gram-Negative Bacterial Pathogens
Newman, C. L., & Stathopoulos, C. (2004) · Critical Reviews in Microbiology · doi:10.1080/10408410490499872 · Cited by 45 · see citing works
Surface anchoring of a bacterial adhesin secreted by the two‐partner secretion pathway
Buscher, A. Z., Grass, S. A., Heuser, J., Roth, R. A., & Geme, J. W. S. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2006.05236.x · Cited by 45 · see citing works
A new expression system for protein crystallization using trimeric coiled-coil adaptors
Alvarez, B. H., Hartmann, M. D., Albrecht, R., et al. (2007) · Protein Engineering Design and Selection · doi:10.1093/protein/gzm071 · Cited by 44 · see citing works
First Analysis of a Bacterial Collagen-Binding Protein with Collagen Toolkits: Promiscuous Binding of YadA to Collagens May Explain How YadA Interferes with Host Processes
Leo, J. C., Elovaara, H., Bihan, D. G., Pugh, N., Kilpinen, S. K., Raynal, N., Skurnik, M., Farndale, R. W., & Goldman, A. (2010) · Infection and Immunity · doi:10.1128/iai.01057-09 · Cited by 43 · see citing works
Self-citation
A transition from strong right-handed to canonical left-handed supercoiling in a conserved coiled-coil segment of trimeric autotransporter adhesins
Alvarez, B. H., Gruber, M., Ursinus, A., Dunin-Horkawicz, S., Lupas, A. N., & Zeth, K. (2010) · Journal of Structural Biology · doi:10.1016/j.jsb.2010.02.009 · Cited by 40 · see citing works
Molecular dynamics simulations of a bacterial autotransporter: NalP fromNeisseria meningitidis
Khalid, S., & Sansom, M. S. P. (2006) · Molecular Membrane Biology · doi:10.1080/09687860600849531 · Cited by 40 · see citing works
GCView: the genomic context viewer for protein homology searches
Grin, I., & Linke, D. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr364 · Cited by 38 · see citing works
Self-citation
Autotransporter β-Domains Have a Specific Function in Protein Secretion beyond Outer-Membrane Targeting
Saurı́, A., Oreshkova, N., Soprova, Z., et al. (2011) · Journal of Molecular Biology · doi:10.1016/j.jmb.2011.07.035 · Cited by 36 · see citing works
Characterization of the Filamentous Hemagglutinin-Like Protein FhaS in Bordetella bronchiseptica
Julio, S. M., & Cotter, P. A. (2005) · Infection and Immunity · doi:10.1128/iai.73.8.4960-4971.2005 · Cited by 36 · see citing works
Intimin-Mediated Export of Passenger Proteins Requires Maintenance of a Translocation-Competent Conformation
Adams, T., Wentzel, A., & Kolmar, H. (2005) · Journal of Bacteriology · doi:10.1128/jb.187.2.522-533.2005 · Cited by 35 · see citing works
Role of the α-Helical Linker of the C-Terminal Translocator in the Biogenesis of the Serine Protease Subfamily of Autotransporters
Kostakioti, M., & Stathopoulos, C. (2006) · Infection and Immunity · doi:10.1128/iai.00103-06 · Cited by 35 · see citing works
YidC Is Involved in the Biogenesis of the Secreted Autotransporter Hemoglobin Protease
Jong, W. S. P., ten Hagen‐Jongman, C. M., Ruijter, E., Orrù, R. V. A., Genevaux, P., & Luirink, J. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.167650 · Cited by 31 · see citing works
The Translocation Domain in Trimeric Autotransporter Adhesins Is Necessary and Sufficient for Trimerization and Autotransportation
Mikula, K. M., Leo, J. C., Łyskowski, A., et al. (2011) · Journal of Bacteriology · doi:10.1128/jb.05322-11 · Cited by 26 · see citing works
Self-citation
Autotransporter proteins, evolution and redefining protein secretion: Response
Henderson, I. R., Cappello, R. E., & Nataro, J. P. (2000) · Trends in Microbiology · doi:10.1016/s0966-842x(00)01884-9 · Cited by 26 · see citing works
ShlB mutants of Serratia marcescens allow uncoupling of activation and secretion of the ShlA hemolysin
Yang, F., & Braun, V. (2000) · International Journal of Medical Microbiology · doi:10.1016/s1438-4221(00)80018-1 · Cited by 24 · see citing works
Sequential translocation of an Escherchia coli two‐partner secretion pathway exoprotein across the inner and outer membranes
Choi, P. S., & Bernstein, H. D. (2009) · Molecular Microbiology · doi:10.1111/j.1365-2958.2009.06993.x · Cited by 20 · see citing works
Autotransporter proteins, evolution and redefining protein secretion: Response
Jacob‐Dubuisson, F., Antoine, R., & Locht, C. (2000) · Trends in Microbiology · doi:10.1016/s0966-842x(00)01885-0 · Cited by 12 · see citing works

Flagged first, then by citations

Sorted by citations

Bacterial autoaggregation
Trunk, T., Bacterial Cell Surface Group, S. F. G. A. E. B., S. Khalil, H., & C. Leo, J. (2018) · AIMS Microbiology · doi:10.3934/microbiol.2018.1.140 · Cited by 444 · see citing works
“A class of proteins that is particularly rich in autoagglutinins is the autotransporter family of Gram-negative bacteria [66].”
BackgroundSelf-citation
Bacterial serine proteases secreted by the autotransporter pathway: classification, specificity, and role in virulence
Ruiz-Perez, F., & Nataro, J. P. (2014) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1355-8 · Cited by 149 · see citing works
<i>Yersinia</i> adhesins: An arsenal for infection
Chauhan, N., Wrobel, A., Skurnik, M., & Leo, J. C. (2016) · PROTEOMICS - CLINICAL APPLICATIONS · doi:10.1002/prca.201600012 · Cited by 57 · see citing works
Self-citation
Genomic insights into cyanobacterial protein translocation systems
Russo, D. A., & Zedler, J. A. Z. (2020) · Biological Chemistry · doi:10.1515/hsz-2020-0247 · Cited by 25 · see citing works

Type I secretion system—it takes three and a substrate
Kanonenberg, K., Spitz, O., Erenburg, I. N., Beer, T., & Schmitt, L. (2018) · FEMS Microbiology Letters · doi:10.1093/femsle/fny094 · Cited by 71 · see citing works
Structural comparison of the transport units of type V secretion systems
Gawarzewski, I., Smits, S. H. J., Schmitt, L., & Jose, J. (2013) · Biological Chemistry · doi:10.1515/hsz-2013-0162 · Cited by 24 · see citing works
Protein secretion in the absence of ATP: the autotransporter, two-partner secretion and chaperone/usher pathways of Gram-negative bacteria (Review)
Thanassi, D. G., Stathopoulos, C., Karkal, A., & Li, H. (2005) · Molecular Membrane Biology · doi:10.1080/09687860500063290 · Cited by 101 · see citing works
The Type 1 secretion pathway — The hemolysin system and beyond
Thomas, S., Holland, I. B., & Schmitt, L. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2013.09.017 · Cited by 210 · see citing works
Multiple Driving Forces Required for Efficient Secretion of Autotransporter Virulence Proteins
Drobnak, I., Braselmann, E., & Clark, P. L. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.629170 · Cited by 26 · see citing works

Authors: Leo, J. C., Grin, I., & Linke, D.
Affiliations: Max Planck Institute for Developmental Biology (DE)
Corresponding author: Linke, Dirk
ORCID: Leo, Jack C.
Grin, Iwan
Linke, Dirk
Venue: Philosophical Transactions of the Royal Society B Biological Sciences
Publisher: The Royal Society
Published: 2012-04-19
Volume: 367
Issue: 1592
Pages: 1088-1101
ISSN: 0962-8436 (ISSN-L)
1471-2970
DOI: 10.1098/rstb.2011.0208
PMC: PMC3297439
OpenAlex: W2135838357
Cited by: 269
References: 123
Citations by year: 2026: 7 · 2025: 16 · 2024: 8 · 2023: 10 · 2022: 16 · 2021: 15 · 2020: 24 · 2019: 31 · 2018: 18 · 2017: 20 · 2016: 24 · 2015: 26 · 2014: 25 · 2013: 20 · 2012: 9
FWCI: 3.13
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
creativecommons.org/licenses/by/3.0/ (vor, 4856 d)
royalsociety.org/journals/ethics-policies/data-sharing-mining/ (tdm)
Locations: Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Nottingham Trent University's Institutional Repository (Nottingham Trent Repository) (acceptedVersion)
Max Planck Institute for Plasma Physics (submittedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Escherichia coli research studies
Life Sciences › Immunology and Microbiology › Microbiology › Bacterial Infections and Vaccines
Keywords: autotransporters, bacterial outer membrane, Gram-negative bacteria, bacterial virulence factors, translocation mechanism, trimeric autotransporter
MeSH terms: Bacterial Outer Membrane Proteins, Bacterial Proteins, Cell Membrane, Gram-Negative Bacteria, Models, Molecular, Protein Structure, Tertiary, Protein Folding, Adhesins, Bacterial, Periplasm, Protein Transport, Virulence Factors, Bacterial Secretion Systems

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Type V secretion: mechanism(s) of autotransport through the bacterial outer membrane

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks