Biogenesis of MalF and the MalFGK2 Maltose Transport Complex in Escherichia coli Requires YidC

Wagner, Samuel; Pop, Ovidiu I.; Haan, Gert Jan; Baars, Louise; Koningstein, Gregory M.; Klepsch, Mirjam; Genevaux, Pierre; Luirink, Joen; Gier, Jan‐Willem de

doi:10.1074/jbc.m801481200

Cited by 59 publications

(23 citation statements)

References 59 publications

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“…This suggests that the Table 1). YidC foldase activity (11)(12)(13)(14) can extend to the periplasmic domains of membrane-anchored proteins. PBP3 insertion is not dependent on YidC.…”

Section: Resultsmentioning

confidence: 99%

“…In addition to its role as an insertase, YidC can also act as a foldase for some proteins such as the sugar transporter LacY (11,12) and mediate the proper assembly of membrane protein complexes such as the MalFGK 2 maltose transporter (13) and the MscL homopentameric pore (14). This feature might be related to the capacity of YidC to interact with the transmembrane domains of proteins that are released by the Sec translocon, whereupon YidC would facilitate the correct assembly and interaction of the transmembrane helices (15,16).…”

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confidence: 99%

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The Escherichia coli Membrane Protein Insertase YidC Assists in the Biogenesis of Penicillin Binding Proteins

et al. 2015

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Membrane proteins need to be properly inserted and folded in the membrane in order to perform a range of activities that are essential for the survival of bacteria. The Sec translocon and the YidC insertase are responsible for the insertion of the majority of proteins into the cytoplasmic membrane. YidC can act in combination with the Sec translocon in the insertion and folding of membrane proteins. However, YidC also functions as an insertase independently of the Sec translocon for so-called YidC-only substrates. In addition, YidC can act as a foldase and promote the proper assembly of membrane protein complexes. Here, we investigate the effect of Escherichia coli YidC depletion on the assembly of penicillin binding proteins (PBPs), which are involved in cell wall synthesis. YidC depletion does not affect the total amount of the specific cell division PBP3 (FtsI) in the membrane, but the amount of active PBP3, as assessed by substrate binding, is reduced 2-fold. A similar reduction in the amount of active PBP2 was observed, while the levels of active PBP1A/1B and PBP5 were essentially similar. PBP1B and PBP3 disappeared from higher-M w bands upon YidC depletion, indicating that YidC might play a role in PBP complex formation. Taken together, our results suggest that the foldase activity of YidC can extend to the periplasmic domains of membrane proteins. IMPORTANCE This study addresses the role of the membrane protein insertase YidC in the biogenesis of penicillin binding proteins (PBPs).PBPs are proteins containing one transmembrane segment and a large periplasmic or extracellular domain, which are involved in peptidoglycan synthesis. We observe that in the absence of YidC, two critical PBPs are not correctly folded even though the total amount of protein in the membrane is not affected. Our findings extend the function of YidC as a foldase for membrane protein (complexes) to periplasmic domains of membrane proteins. Membrane proteins need to be properly inserted and folded in the membrane in order to be functional. The Escherichia coli Sec translocon and the YidC insertase are involved in the insertion of the majority of membrane proteins into the membrane. YidC can act in combination with the Sec translocon to facilitate the insertion and folding of membrane proteins, but can also function on its own as an insertase for so-called YidC-only substrates (1). Although YidC was discovered more than 13 years ago (2, 3), only a few YidC-only substrates are known at present. YidC-only substrates have short translocated regions and include the F 1 F 0 -ATPase subunit c (4-7), the M13 phage procoat protein (8), the mechano-sensing MscL protein (9), the Sci-1 type VI secretion system subunit TssL (10), and the Pf3 coat protein (3).In addition to its role as an insertase, YidC can also act as a foldase for some proteins such as the sugar transporter LacY (11, 12) and mediate the proper assembly of membrane protein complexes such as the MalFGK 2 maltose transporter (13) and the MscL homopentameric pore (14). This ...

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“…This suggests that the Table 1). YidC foldase activity (11)(12)(13)(14) can extend to the periplasmic domains of membrane-anchored proteins. PBP3 insertion is not dependent on YidC.…”

Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

The Escherichia coli Membrane Protein Insertase YidC Assists in the Biogenesis of Penicillin Binding Proteins

et al. 2015

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“…The extent and duration of the contact with YidC may depend on the characteristics and context of the individual TM in the substrate nascent chain. The first three TMs in the polytopic membrane proteins MtlA (7) and MalF (41) have been shown to contact YidC simultaneously, suggesting that YidC also functions as a platform for the assembly of complex IMPs. Possibly, YidC TM3 functions in the initial recognition of substrate TMs before relocating them for folding and assembly to other regions in YidC that remain to be determined.…”

Section: Discussionmentioning

confidence: 99%

The Conserved Third Transmembrane Segment of YidC Contacts Nascent Escherichia coli Inner Membrane Proteins

Yu¹,

Koningstein²,

Pop³

et al. 2008

Journal of Biological Chemistry

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Escherichia coli YidC is a polytopic inner membrane protein that plays an essential and versatile role in the biogenesis of inner membrane proteins. YidC functions in Sec-dependent membrane insertion but acts also independently as a separate insertase for certain small membrane proteins. We have used a site-specific cross-linking approach to show that the conserved third transmembrane segment of YidC contacts the transmembrane domains of both nascent Sec-dependent and -independent substrates, indicating a generic recognition of insertion intermediates by YidC. Our data suggest that specific residues of the third YidC transmembrane segment ␣-helix is oriented toward the transmembrane domains of nascent inner membrane proteins that, in contrast, appear quite flexibly positioned at this stage in biogenesis.

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“…YidC, docked at the SecY lateral gate (29), interacts with a subset of transmembrane segments as they exit the translocon. YidC is believed to enable folding of the proteins with correct topology into an intrinsically stable conformation (27,39,40), as well as stabilization of unbalanced transmembrane segments as they are folded (25). Folded membrane proteins are then released from YidC into the lipid bilayer.…”

Section: Discussionmentioning

confidence: 99%

Identification of YidC Residues That Define Interactions with the Sec Apparatus

Boyd

Reindl

et al. 2013

Journal of Bacteriology

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In bacteria, a subset of membrane proteins insert into the membrane via the Sec apparatus with the assistance of the widely conserved essential membrane protein insertase YidC. After threading into the SecYEG translocon, transmembrane segments of nascent proteins are thought to exit the translocon via a lateral gate in SecY, where YidC facilitates their transfer into the lipid bilayer. Interactions between YidC and components of the Sec apparatus are critical to its function. The first periplasmic loop of YidC interacts directly with SecF. We sought to identify the regions or residues of YidC that interact with SecY or with additional components of the Sec apparatus other than SecDF. Using a synthetic lethal screen, we identified residues of YidC that, when mutated, led to dependence on SecDF for viability. Each residue identified is highly conserved among YidC homologs; most lie within transmembrane domains. Overexpression of SecY in the presence of two YidC mutants partially rescued viability in the absence of SecDF, suggesting that the corresponding wild-type YidC residues (G355 and M471) participate in interactions, direct or indirect, with SecY. Staphylococcus aureus YidC complemented depletion of YidC, but not of SecDF, in Escherichia coli. G355 of E. coli YidC is invariant in S. aureus YidC, suggesting that this highly conserved glycine serves a conserved function in interactions with SecY. This study demonstrates that transmembrane residues are critical in YidC interactions with the Sec apparatus and provides guidance on YidC residues of interest for future structure-function analyses.

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Biogenesis of MalF and the MalFGK2 Maltose Transport Complex in Escherichia coli Requires YidC

Cited by 59 publications

References 59 publications

The Escherichia coli Membrane Protein Insertase YidC Assists in the Biogenesis of Penicillin Binding Proteins

The Escherichia coli Membrane Protein Insertase YidC Assists in the Biogenesis of Penicillin Binding Proteins

The Conserved Third Transmembrane Segment of YidC Contacts Nascent Escherichia coli Inner Membrane Proteins

Identification of YidC Residues That Define Interactions with the Sec Apparatus

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