Structural biology of the chaperone–usher pathway of pilus biogenesis

Gabriel Waksman; Scott J. Hultgren

doi:10.1038/nrmicro2220

journal article Open Access Oct 12, 2009

Structural biology of the chaperone–usher pathway of pilus biogenesis

Gabriel Waksman

Scott J. Hultgren

Nature Reviews Microbiology Vol. 7 No. 11 pp. 765-774 · Springer Science and Business Media LLC

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References

76

[1]

Architectures and biogenesis of non-flagellar protein appendages in Gram-negative bacteria

Rémi Fronzes, Han Remaut, Gabriel Waksman

The EMBO Journal 2008 10.1038/emboj.2008.155

[2]

Sauer, F. G., Remaut, H., Hultgren, S. J. & Waksman, G. Fiber assembly by the chaperone-usher pathway. Biochim. Biophys. Acta 1694, 259–267 (2004). 10.1016/j.bbamcr.2004.02.010

[3]

Barnhart, M. M. et al. PapD-like chaperones provide the missing information for folding of pilin proteins. Proc. Natl Acad. Sci. USA 97, 7709–7714 (2000). 10.1073/pnas.130183897

[4]

Outer-membrane PapC molecular usher discriminately recognizes periplasmic chaperone-pilus subunit complexes.

K W Dodson, F Jacob-Dubuisson, R T Striker et al.

Proceedings of the National Academy of Sciences 1993 10.1073/pnas.90.8.3670

[5]

Thanassi, D. G. et al. The PapC usher forms an oligomeric channel: implications for pilus biogenesis across the outer membrane. Proc. Natl Acad. Sci. USA 95, 3146–3151 (1998). 10.1073/pnas.95.6.3146

[6]

Evolution of the Chaperone/Usher Assembly Pathway: Fimbrial Classification Goes Greek

Sean-Paul Nuccio, Andreas J. Bäumler

Microbiology and Molecular Biology Reviews 2007 10.1128/mmbr.00014-07

[7]

Kuehn, M. J., Heuser, J., Normark, S. & Hultgren, S. J. P pili in uropathogenic E. coli are composite fibres with distinct fibrillar adhesive tips. Nature 356, 252–255 (1992). 10.1038/356252a0

[8]

Biogenesis of E. coli Pap pili: PapH, a minor pilin subunit involved in cell anchoring and length modulation

Monica Båga, Mari Norgren, Staffan Normark

Cell 1987 10.1016/0092-8674(87)90565-4

[9]

Molecular mechanism of P pilus termination in uropathogenic Escherichia coli

Denis Verger, Eric Miller, Han Remaut et al.

EMBO reports 2006 10.1038/sj.embor.7400833

[10]

Hahn, E. et al. Exploring the 3D molecular architecture of Escherichia coli type 1 pili. J. Mol. Biol. 323, 845–857 (2002). 10.1016/s0022-2836(02)01005-7

[11]

Hultgren, S. J. et al. The PapG adhesin of uropathogenic Escherichia coli contains separate regions for receptor binding and for the incorporation into the pilus. Proc. Natl Acad. Sci. USA 86, 4357–4361 (1989). 10.1073/pnas.86.12.4357

[12]

Jones, C. H., Danese, P. N., Pinkner, J. S., Silhavy, T. J. & Hultgren, S. J. The chaperone-assisted membrane release and folding pathway is sensed by two signal transduction systems. EMBO J. 16, 6394–6406 (1997). 10.1093/emboj/16.21.6394

[13]

Vetsch, M. et al. Pilus chaperones represent a new type of protein-folding catalyst. Nature 431, 329–333 (2004). 10.1038/nature02891

[14]

Holmgren, A. & Branden, C. I. Crystal structure of chaperone protein PapD reveals an immunoglobulin fold. Nature 342, 248–251 (1989). This study elucidates the structure of a periplasmic chaperone. 10.1038/342248a0

[15]

Kuehn, M. J. et al. Structural basis of pilus subunit recognition by the PapD chaperone. Science 262, 1234–1241 (1993). This paper describes the first structure of a complex between a periplasmic chaperone and a peptide derived from a pilin subunit. 10.1126/science.7901913

[16]

Slonim, L. N., Pinkner, J. S., Branden, C. I. & Hultgren, S. J. Interactive surface in the PapD chaperone cleft is conserved in pilus chaperone superfamily and essential in subunit recognition and assembly. EMBO J. 11, 4747–4756 (1992). 10.1002/j.1460-2075.1992.tb05580.x

[17]

Choudhury, D. et al. X-ray structure of the FimC-FimH chaperone-adhesin complex from uropathogenic Escherichia coli. Science 285, 1061–1066 (1999). 10.1126/science.285.5430.1061

[18]

Sauer, F. G. et al. Structural basis of chaperone function and pilus biogenesis. Science 285, 1058–1061 (1999). This article and reference 17 present the structures of chaperone–subunit complexes and formulate the concepts of donor strand complementation for chaperone function and donor strand exchange for subunit assembly. Reference 17 also provides insights into receptor recognition by the type 1 pilus, as it contains the structure of the FimH lectin domain. 10.1126/science.285.5430.1058

[19]

Bann, J. G., Pinkner, J. S., Frieden, C. & Hultgren, S. J. Catalysis of protein folding by chaperones in pathogenic bacteria. Proc. Natl Acad. Sci. USA 101, 17389–17393 (2004). 10.1073/pnas.0408072101

[20]

Hung., D. L., Knight, S. D., Woods, R. M., Pinkner, J. S. & Hultgren, S. J. Molecular basis of two subfamilies of immunoglobulin-like chaperones. EMBO J. 15, 3792–3805 (1996). 10.1002/j.1460-2075.1996.tb00753.x

[21]

Zavialov, A. V. et al. Structure and biogenesis of the capsular F1 antigen from Yersinia pestis: preserved folding energy drives fiber formation. Cell 113, 587–596 (2003). 10.1016/s0092-8674(03)00351-9

[22]

Remaut, H. et al. Donor-strand exchange in chaperone-assisted pilus assembly proceeds through a concerted β strand displacement mechanism. Mol. Cell 22, 831–842 (2006). This paper presents the first evidence that donor strand exchange occurs through a 'zip-in, zip-out' mechanism that is initiated at the P5 pocket. 10.1016/j.molcel.2006.05.033

[23]

Anderson, K. L. et al. An atomic resolution model for assembly, architecture, and function of the Dr adhesins. Mol. Cell 15, 647–657 (2004). 10.1016/j.molcel.2004.08.003

[24]

Sauer, F. G., Pinkner, J. S., Waksman, G. & Hultgren, S. J. Chaperone priming of pilus subunits facilitates a topological transition that drives fiber formation. Cell 111, 543–551 (2002). This paper and reference 21 reveal the structures of a ternary complex containing a subunit in donor strand complementation with its cognate chaperone and the same subunit in donor strand exchange with a second subunit. Together with reference 17, these studies validate the concept of donor strand exchange. 10.1016/s0092-8674(02)01050-4

[25]

Vetsch, M. et al. Mechanism of fibre assembly through the chaperone-usher pathway. EMBO Rep. 7, 734–738 (2006). 10.1038/sj.embor.7400722

[26]

Lindberg, F., Lund, B., Johansson, L. & Normark, S. Localization of the receptor-binding protein adhesin at the tip of the bacterial pilus. Nature 328, 84–87 (1987). 10.1038/328084a0

[27]

Jacob-Dubuisson, F., Heuser, J., Dodson, K., Normark, S. & Hultgren, S. Initiation of assembly and association of the structural elements of a bacterial pilus depend on two specialized tip proteins. EMBO J. 12, 837–847 (1993). 10.1002/j.1460-2075.1993.tb05724.x

[28]

Striker, R., Jacob-Dubuisson, F., Freiden, C. & Hultgren, S. J. Stable fiber-forming and nonfiber-forming chaperone-subunit complexes in pilus biogenesis. J. Biol. Chem. 269, 12233–12239 (1994). 10.1016/s0021-9258(17)32706-0

[29]

Lee, Y. M., Dodson, K. W. & Hultgren, S. J. Adaptor function of PapF depends on donor strand exchange in P-pilus biogenesis of Escherichia coli. J. Bacteriol. 189, 5276–5283 (2007). 10.1128/jb.01648-06

[30]

Rose, R. J. et al. Unraveling the molecular basis of subunit specificity in P pilus assembly by mass spectrometry. Proc. Natl Acad. Sci. USA 105, 12873–12878 (2008). 10.1073/pnas.0802177105

[31]

Verger, D. et al. Structural determinants of polymerization reactivity of the P pilus adaptor subunit PapF. Structure 16, 1724–1731 (2008). 10.1016/j.str.2008.08.012

[32]

Saulino, E. T., Thanassi, D. G., Pinkner, J. S. & Hultgren, S. J. Ramifications of kinetic partitioning on usher-mediated pilus biogenesis. EMBO J. 17, 2177–2185 (1998). 10.1093/emboj/17.8.2177

[33]

Nishiyama, M. et al. Structural basis of chaperone-subunit complex recognition by the type 1 pilus assembly platform FimD. EMBO J. 24, 2075–2086 (2005). This paper describes the first structure of the FimD N-terminal domain bound to a chaperone–subunit complex. 10.1038/sj.emboj.7600693

[34]

Nishiyama, M., Ishikawa, T., Rechsteiner, H. & Glockshuber, R. Reconstitution of pilus assembly reveals a bacterial outer membrane catalyst. Science 320, 376–379 (2008). This paper describes the first in vitro reconstitution of pilus biogenesis from purified components. 10.1126/science.1154994

[35]

Remaut, H. et al. Fibre formation across the bacterial outer membrane by the chaperone/usher pathway. Cell 133, 640–652 (2008). This paper describes the structure of the translocation usher pore and proposes a general mechanism of usher function on the basis of the pore structure and a cryo-EM structure of the FimD usher bound to a secretion intermediate. 10.1016/j.cell.2008.03.033

[36]

Li, H. et al. The outer membrane usher forms a twin-pore secretion complex. J. Mol. Biol. 344, 1397–1407 (2004). 10.1016/j.jmb.2004.10.008

[37]

So, S. S. & Thanassi, D. G. Analysis of the requirements for pilus biogenesis at the outer membrane usher and the function of the usher C-terminus. Mol. Microbiol. 60, 364–375 (2006). 10.1111/j.1365-2958.2006.05111.x

[38]

Huang, Y., Smith, B. S., Chen, L. X., Baxter, R. H. & Deisenhofer, J. Insights into pilus assembly and secretion from the structure and functional characterization of usher PapC. Proc. Natl Acad. Sci. USA 106, 7403–7407 (2009). 10.1073/pnas.0902789106

[39]

Thanassi, D. G., Stathopoulos, C., Dodson, K., Geiger, D. & Hultgren, S. J. Bacterial outer membrane ushers contain distinct targeting and assembly domains for pilus biogenesis. J. Bacteriol. 184, 6260–6269 (2002). 10.1128/jb.184.22.6260-6269.2002

[40]

Nishiyama, M., Vetsch, M., Puorger, C., Jelesarov, I. & Glockshuber, R. Identification and characterization of the chaperone-subunit complex-binding domain from the type 1 pilus assembly platform FimD. J. Mol. Biol. 330, 513–525 (2003). 10.1016/s0022-2836(03)00591-6

[41]

Capitani, G., Eidam, O. & Grutter, M. G. Evidence for a novel domain of bacterial outer membrane ushers. Proteins 65, 816–823 (2006). 10.1002/prot.21147

[42]

Ng, T. W., Akman, L., Osisami, M. & Thanassi, D. G. The usher N terminus is the initial targeting site for chaperone-subunit complexes and participates in subsequent pilus biogenesis events. J. Bacteriol. 186, 5321–5331 (2004). 10.1128/jb.186.16.5321-5331.2004

[43]

Eidam, O., Dworkowski, F. S., Glockshuber, R., Grutter, M. G. & Capitani, G. Crystal structure of the ternary FimC-FimFt-FimDN complex indicates conserved pilus chaperone-subunit complex recognition by the usher FimD. FEBS Lett. 582, 651–655 (2008). 10.1016/j.febslet.2008.01.030

[44]

Specific residues in the N‐terminal domain of FimH stimulate type 1 fimbriae assembly in Escherichia coli following the initial binding of the adhesin to FimD usher

Diana Munera, Carmen Palomino, Luis Ángel Fernández

Molecular Microbiology 2008 10.1111/j.1365-2958.2008.06325.x

[45]

Recognition of the N‐terminal lectin domain of FimH adhesin by the usher FimD is required for type 1 pilus biogenesis

Diana Munera, Scott Hultgren, Luis Ángel Fernández

Molecular Microbiology 2007 10.1111/j.1365-2958.2007.05657.x

[46]

Saulino, E. T., Bullitt, E. & Hultgren, S. J. Snapshots of usher-mediated protein secretion and ordered pilus assembly. Proc. Natl Acad. Sci. USA 97, 9240–9245 (2000). 10.1073/pnas.160070497

[47]

Jacob-Dubuisson, F., Striker, R. & Hultgren, S. J. Chaperone-assisted self-assembly of pili independent of cellular energy. J. Biol. Chem. 269, 12447–12455 (1994). 10.1016/s0021-9258(18)99895-9

[48]

Zavialov, A. V. et al. Resolving the energy paradox of chaperone/usher-mediated fibre assembly. Biochem. J. 389, 685–694 (2005). 10.1042/bj20050426

[49]

Induction and Evasion of Host Defenses by Type 1-Piliated Uropathogenic Escherichia coli

Matthew A. Mulvey, Yolanda S. Lopez-Boado, Carole L. Wilson et al.

Science 1998 10.1126/science.282.5393.1494

[50]

Type 1 fimbriae and extracellular polysaccharides are preeminent uropathogenic Escherichia coli virulence determinants in the murine urinary tract

Farah K. Bahrani‐Mougeot, Eric L. Buckles, C. V. Lockatell et al.

Molecular Microbiology 2002 10.1046/j.1365-2958.2002.03078.x

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Published: Oct 12, 2009
Vol/Issue: 7(11)
Pages: 765-774
License: View

Authors

G

Gabriel Waksman

Institute of Structural and Molecular Biology

S

Scott J. Hultgren

Washington University in St. Louis

Cite This Article

Gabriel Waksman, Scott J. Hultgren (2009). Structural biology of the chaperone–usher pathway of pilus biogenesis. Nature Reviews Microbiology, 7(11), 765-774. https://doi.org/10.1038/nrmicro2220

Structural biology of the chaperone–usher pathway of pilus biogenesis

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