PapD Chaperone Function in Pilus Biogenesis Depends on Oxidant and Chaperone-like Activities of DsbA

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1994 Nov 22

PMID 7972100

Citations 54

Authors

F Jacob-Dubuisson

J Pinkner

Z Xu

R Striker

A Padmanhaban

S J Hultgren

Affiliations

Soon will be listed here.

Abstract

Adhesive P pili of uropathogenic Escherichia coli were not assembled by a strain that lacks the periplasmic disulfide isomerase DsbA. This defect was mostly attributed to the immunoglobulin-like pilus chaperone PapD, which possesses an unusual intrasheet disulfide bond between the last two beta-strands of its CD4-like carboxyl-terminal domain. The DsbA-dependent formation of this disulfide bond was critical for PapD's proper folding in vivo. Interestingly, the absence of the disulfide bond did not prevent PapD from folding in vitro or from forming a complex with the pilus adhesin in vitro. We suggest that DsbA maintains nascently translocated PapD in a folding-competent conformation prior to catalyzing disulfide bond formation, acting both as an oxidant and in a chaperone-like fashion. Disulfide bond formation in pilus subunits was also mediated by DsbA even in the absence of PapD. However, the ability of pilus subunits to achieve native-like conformations in vivo depended on PapD. These results suggest that a productive folding pathway for subunits requires sequential interactions with DsbA and the PapD chaperone.

Citing Articles

Unveiling the versatility of the thioredoxin framework: Insights from the structural examination of DsbA1.

Penning S, Hong Y, Cunliffe T, Hor L, Totsika M, Paxman J Comput Struct Biotechnol J. 2024; 23:4324-4336.

PMID: 39697679 PMC: 11653150. DOI: 10.1016/j.csbj.2024.11.034.

A Buried Water Network Modulates the Activity of the Disulphide Catalyst DsbA.

Wang G, Qin J, Verderosa A, Hor L, Santos-Martin C, Paxman J Antioxidants (Basel). 2023; 12(2).

PMID: 36829940 PMC: 9952396. DOI: 10.3390/antiox12020380.

Pleiotropic roles of late embryogenesis abundant proteins of against oxidation and desiccation.

Liu Y, Zhang C, Wang Z, Lin M, Wang J, Wu M Comput Struct Biotechnol J. 2021; 19:3407-3415.

PMID: 34188783 PMC: 8213827. DOI: 10.1016/j.csbj.2021.05.051.

Protein Disulfide Exchange by the Intramembrane Enzymes DsbB, DsbD, and CcdA.

Bushweller J J Mol Biol. 2020; 432(18):5091-5103.

PMID: 32305461 PMC: 7485265. DOI: 10.1016/j.jmb.2020.04.008.

Oxidoreductase disulfide bond proteins DsbA and DsbB form an active redox pair in Chlamydia trachomatis, a bacterium with disulfide dependent infection and development.

Christensen S, Halili M, Strange N, Petit G, Huston W, Martin J PLoS One. 2019; 14(9):e0222595.

PMID: 31536549 PMC: 6752827. DOI: 10.1371/journal.pone.0222595.

References

Missiakas D, Georgopoulos C, Raina S . The Escherichia coli dsbC (xprA) gene encodes a periplasmic protein involved in disulfide bond formation. EMBO J. 1994; 13(8):2013-20. PMC: 395044. DOI: 10.1002/j.1460-2075.1994.tb06471.x. View

Puig A, Gilbert H . Protein disulfide isomerase exhibits chaperone and anti-chaperone activity in the oxidative refolding of lysozyme. J Biol Chem. 1994; 269(10):7764-71. View

Russel M, Model P . The role of thioredoxin in filamentous phage assembly. Construction, isolation, and characterization of mutant thioredoxins. J Biol Chem. 1986; 261(32):14997-5005. View

Collier D, Bankaitis V, Weiss J, Bassford Jr P . The antifolding activity of SecB promotes the export of the E. coli maltose-binding protein. Cell. 1988; 53(2):273-83. DOI: 10.1016/0092-8674(88)90389-3. View

Lindberg F, Tennent J, Hultgren S, Lund B, Normark S . PapD, a periplasmic transport protein in P-pilus biogenesis. J Bacteriol. 1989; 171(11):6052-8. PMC: 210471. DOI: 10.1128/jb.171.11.6052-6058.1989. View

Holmgren A, Branden C . Crystal structure of chaperone protein PapD reveals an immunoglobulin fold. Nature. 1989; 342(6247):248-51. DOI: 10.1038/342248a0. View

Simons B, Rathman P, Malij C, Oudega B, de Graaf F . The penultimate tyrosine residue of the K99 fibrillar subunit is essential for stability of the protein and its interaction with the periplasmic carrier protein. FEMS Microbiol Lett. 1990; 55(1-2):107-12. DOI: 10.1016/0378-1097(90)90177-r. View

Bardwell J, McGovern K, Beckwith J . Identification of a protein required for disulfide bond formation in vivo. Cell. 1991; 67(3):581-9. DOI: 10.1016/0092-8674(91)90532-4. View

Kuehn M, Normark S, Hultgren S . Immunoglobulin-like PapD chaperone caps and uncaps interactive surfaces of nascently translocated pilus subunits. Proc Natl Acad Sci U S A. 1991; 88(23):10586-90. PMC: 52974. DOI: 10.1073/pnas.88.23.10586. View

10.

Gething M, Sambrook J . Protein folding in the cell. Nature. 1992; 355(6355):33-45. DOI: 10.1038/355033a0. View

11.

Kamitani S, Akiyama Y, Ito K . Identification and characterization of an Escherichia coli gene required for the formation of correctly folded alkaline phosphatase, a periplasmic enzyme. EMBO J. 1992; 11(1):57-62. PMC: 556425. DOI: 10.1002/j.1460-2075.1992.tb05027.x. View

12.

Kuehn M, Heuser J, Normark S, Hultgren S . P pili in uropathogenic E. coli are composite fibres with distinct fibrillar adhesive tips. Nature. 1992; 356(6366):252-5. DOI: 10.1038/356252a0. View

13.

Holmgren A, Kuehn M, Branden C, Hultgren S . Conserved immunoglobulin-like features in a family of periplasmic pilus chaperones in bacteria. EMBO J. 1992; 11(4):1617-22. PMC: 556611. DOI: 10.1002/j.1460-2075.1992.tb05207.x. View

14.

Peek J, Taylor R . Characterization of a periplasmic thiol:disulfide interchange protein required for the functional maturation of secreted virulence factors of Vibrio cholerae. Proc Natl Acad Sci U S A. 1992; 89(13):6210-4. PMC: 402152. DOI: 10.1073/pnas.89.13.6210. View

15.

Yu J, Webb H, Hirst T . A homologue of the Escherichia coli DsbA protein involved in disulphide bond formation is required for enterotoxin biogenesis in Vibrio cholerae. Mol Microbiol. 1992; 6(14):1949-58. DOI: 10.1111/j.1365-2958.1992.tb01368.x. View

16.

Akiyama Y, Kamitani S, Kusukawa N, Ito K . In vitro catalysis of oxidative folding of disulfide-bonded proteins by the Escherichia coli dsbA (ppfA) gene product. J Biol Chem. 1992; 267(31):22440-5. View

17.

Slonim L, Pinkner J, Branden C, Hultgren S . Interactive surface in the PapD chaperone cleft is conserved in pilus chaperone superfamily and essential in subunit recognition and assembly. EMBO J. 1992; 11(13):4747-56. PMC: 556950. DOI: 10.1002/j.1460-2075.1992.tb05580.x. View

18.

Gong M, Makowski L . Helical structure of P pili from Escherichia coli. Evidence from X-ray fiber diffraction and scanning transmission electron microscopy. J Mol Biol. 1992; 228(3):735-42. DOI: 10.1016/0022-2836(92)90860-m. View

19.

Bardwell J, Lee J, Jander G, Martin N, Belin D, Beckwith J . A pathway for disulfide bond formation in vivo. Proc Natl Acad Sci U S A. 1993; 90(3):1038-42. PMC: 45806. DOI: 10.1073/pnas.90.3.1038. View

20.

Dill K, Fiebig K, Chan H . Cooperativity in protein-folding kinetics. Proc Natl Acad Sci U S A. 1993; 90(5):1942-6. PMC: 45996. DOI: 10.1073/pnas.90.5.1942. View