A Conserved Aromatic Residue in the Autochaperone Domain of the Autotransporter Hbp Is Critical for Initiation of Outer Membrane Translocation

Soprova, Zora; Saurı́, Ana; Ulsen, Peter van; Tame, J.R.H.; Blaauwen, Tanneke den; Jong, Wouter S. P.; Luirink, Joen

doi:10.1074/jbc.m110.180505

Cited by 54 publications

(82 citation statements)

References 48 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…We then investigated the ability of the meningococcal TpsBs to secrete TPS domains of N. lactamica, since this is a closely related bacterial species that occupies the same niche in the human body. Like in N. meningitidis, several TPS systems have been identified in N. lactamica, and not all appear to have a dedicated TpsB encoded (35,36). Furthermore, sequence comparisons of TPS domains showed that the systems in N. meningitidis and N. lactamica are related (see Table S2 in the supplemental material).…”

Section: Resultsmentioning

confidence: 99%

System Specificity of the TpsB Transporters of Coexpressed Two-Partner Secretion Systems of Neisseria meningitidis

Rahman

Ulsen

2012

Journal of Bacteriology

View full text Add to dashboard Cite

The two-partner secretion (TPS) systems of Gram-negative bacteria consist of a large secreted exoprotein (TpsA) and a transporter protein (TpsB) located in the outer membrane. TpsA targets TpsB for transport across the membrane via its ϳ30-kDa TPS domain located at its N terminus, and this domain is also the minimal secretory unit. Neisseria meningitidis genomes encode up to five TpsAs and two TpsBs. Sequence alignments of TPS domains suggested that these are organized into three systems, while there are two TpsBs, which raised questions on their system specificity. We show here that the TpsB2 transporter of Neisseria meningitidis is able to secrete all types of TPS domains encoded in N. meningitidis and the related species Neisseria lactamica but not domains of Haemophilus influenzae and Pseudomonas aeruginosa. In contrast, the TpsB1 transporter seemed to be specific for its cognate N. meningitidis system and did not secrete the TPS domains of other meningococcal systems. However, TpsB1 did secrete the TPS2b domain of N. lactamica, which is related to the meningococcal TPS2 domains. Apparently, the secretion depends on specific sequences within the TPS domain rather than the overall TPS domain structure.

show abstract

Section: Resultsmentioning

confidence: 99%

System Specificity of the TpsB Transporters of Coexpressed Two-Partner Secretion Systems of Neisseria meningitidis

Rahman

Ulsen

2012

Journal of Bacteriology

View full text Add to dashboard Cite

show abstract

“…Position 453 lies within the first predicted ␤-strand of the N-terminal extracellular domain (D00) of the passenger Thus, the introduced double HA tag presumably leads to misfolding of the D00 domain. Tsai et al (13) assumed that this domain could function as an autochaperone domain as it was described for classical monomeric autotransporters (31)(32)(33). Such domains initiate the vectorial export of the passenger by forming a hairpin intermediate and improve transport efficiency.…”

Section: Intha453 Is Expressed At the Wild Type Level And The ␤-Barrementioning

confidence: 99%

The Inverse Autotransporter Intimin Exports Its Passenger Domain via a Hairpin Intermediate

Oberhettinger

Leo

Linke

et al. 2015

Journal of Biological Chemistry

View full text Add to dashboard Cite

Background:Intimin exports its C-terminal passenger domain through an N-terminal ␤-barrel onto the bacterial surface. Results: Insertion of an epitope tag at the very N terminus of the passenger domain stalls the export of the passenger. Conclusion:The intimin passenger adopts a hairpin conformation during translocation. Significance: Our results confirm the hairpin model of inverse autotransport where the passenger is translocated from the N to the C terminus.

show abstract

“…sory factors assisting in translocation of passenger domains across the OM (5,22) and stabilizes these otherwise transient protein-protein interactions in whole cells. After cross-linking, E. coli cells expressing Pet48aa, Pet1HA, and Pet1HA-FLAG were harvested, spheroplasted, and lysed, and membrane proteins were co-purified with immobilized anti-Pet passenger domain antibody.…”

Section: Native Cys Residues Are Not Required For Secretion or Foldinmentioning

confidence: 99%

Size and Conformation Limits to Secretion of Disulfide-bonded Loops in Autotransporter Proteins

Leyton

Sevastsyanovich

Browning

et al. 2011

Journal of Biological Chemistry

View full text Add to dashboard Cite

Background: There is a general paucity of cysteine residues within the passenger domains of autotransporter proteins. Results: Distantly spaced cysteines forming disulfide-bonded loops or those enclosing structural elements are secretion-incompetent. Conclusion: Only closely spaced cysteine pairs are compatible with the autotransporter pathway. Significance: Secretion of folded peptides by the autotransporter pathway is limited; hence autotransporters lack large disulfide-bonded loops to remain secretion-competent.Autotransporters are a superfamily of virulence factors typified by a channel-forming C terminus that facilitates translocation of the functional N-terminal passenger domain across the outer membrane of Gram-negative bacteria. This final step in the secretion of autotransporters requires a translocation-competent conformation for the passenger domain that differs markedly from the structure of the fully folded secreted protein.The nature of the translocation-competent conformation remains controversial, in particular whether the passenger domain can adopt secondary structural motifs, such as disulfide-bonded segments, while maintaining a secretion-competent state. Here, we used the endogenous and closely spaced cysteine residues of the plasmid-encoded toxin (Pet) from enteroaggregative Escherichia coli to investigate the effect of disulfide bond-induced folding on translocation of an autotransporter passenger domain. We reveal that rigid structural elements within disulfide-bonded segments are resistant to autotransporter-mediated secretion. We define the size limit of disulfide-bonded segments tolerated by the autotransporter system demonstrating that, when present, cysteine pairs are intrinsically closely spaced to prevent congestion of the translocator pore by large disulfide-bonded regions. These latter data strongly support the hairpin mode of autotransporter biogenesis.Gram-negative bacteria possess seven secretion pathways (numbered I-VI and the chaperone-usher pathway) that facilitate navigation of secreted proteins through the inner membrane, periplasm, and outer membrane (OM).2 These pathways generally use specialized machineries that span the width of the cell envelope and that differ in complexity, structural features, and mechanism of protein translocation. At first glance, the simplicity of the type Va secretion pathway appeared to be the exception; all the functional elements required for secretion appeared to be contained within a single protein with the N-terminal signal peptide mediating inner membrane translocation, the central passenger domain being the secreted functional moiety, and the C terminus forming a ␤-barrel structure in the OM, the latter element being essential for passenger domain translocation to the bacterial cell surface. Accordingly, the superfamily of proteins that exploit this pathway for their delivery to the surface of Gram-negative bacteria was termed autotransporters (ATs) (1). However, recent studies demonstrating that passenger domain secretion requires the ...

show abstract

A Conserved Aromatic Residue in the Autochaperone Domain of the Autotransporter Hbp Is Critical for Initiation of Outer Membrane Translocation

Cited by 54 publications

References 48 publications

System Specificity of the TpsB Transporters of Coexpressed Two-Partner Secretion Systems of Neisseria meningitidis

System Specificity of the TpsB Transporters of Coexpressed Two-Partner Secretion Systems of Neisseria meningitidis

The Inverse Autotransporter Intimin Exports Its Passenger Domain via a Hairpin Intermediate

Size and Conformation Limits to Secretion of Disulfide-bonded Loops in Autotransporter Proteins

Contact Info

Product

Resources

About