YidC Protein, a Molecular Chaperone for LacY Protein Folding via the SecYEG Protein Machinery

Zhu, Lu; Kaback, H. Ronald; Dalbey, Ross E.

doi:10.1074/jbc.m113.491613

Cited by 43 publications

(29 citation statements)

References 76 publications

(88 reference statements)

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“…Depletion of YidC leads to wider cells that have a division defect, which is in accordance with a reduction in function of the elongation and division specific class B transpeptidases PBP2 and PBP3. Importantly, whereas earlier reports already identified YidC as a foldase/ chaperone for proteins with multiple transmembrane segments (11)(12)(13)(14), we report here a role for YidC in the correct assembly of periplasmic domains of membrane proteins. We observed that the absence of YidC hardly affects the total amount of PBP3 in the membrane but more than halves the amount of correctly folded PBP3, as determined by substrate binding.…”

Section: Resultsmentioning

confidence: 39%

“…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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Section: Resultsmentioning

confidence: 39%

“…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%

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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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“…In the holo-complex, YidC functions to promote the removal of transmembrane segments of inserting membrane proteins from the Sec channel (78), facilitates their integration into the lipid bilayer (79), and acts as an assembly site for multispanning membrane proteins (80). As part of its folding function, YidC plays a direct role in the helix-helix packing of membrane proteins (81,82). This explains why YidC is required for the folding, but not insertion, of LacY (81, 82) and MalF (83) and is required for the assembly of the maltose transporter MalFGK (83).…”

Section: Yidc Familymentioning

confidence: 99%

YidC/Alb3/Oxa1 Family of Insertases

Hennon

Soman

Zhu

et al. 2015

Journal of Biological Chemistry

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The YidC/Alb3/Oxa1 family functions in the insertion and folding of proteins in the bacterial cytoplasmic membrane, the chloroplast thylakoid membrane, and the mitochondrial inner membrane. All members share a conserved region composed of five transmembrane regions. These proteins mediate membrane insertion of an assorted group of proteins, ranging from respiratory subunits in the mitochondria and light-harvesting chlorophyll-binding proteins in chloroplasts to ATP synthase subunits in bacteria. This review discusses the YidC/Alb3/Oxa1 protein family as well as their function in membrane insertion and two new structures of the bacterial YidC, which suggest a mechanism for membrane insertion by this family of insertases.In all cells, membrane proteins play crucial roles in energy production, substrate transport, signaling, and metabolite exchange. They function as ATPases, photosynthetic complexes, chemosensors, and permeases. Membrane proteins make up 25-30% of the proteins in a cell and comprise over 50% of known drug targets. To assemble proteins into the membrane lipid bilayer, translocation and insertion machineries are required in cells. The Sec translocase is the major translocase that inserts proteins into and across the endoplasmic reticulum of eukaryotic cells, the cytoplasmic membrane of bacterial and archaeal cells, and the thylakoid membrane of plants. When translocating proteins across the membrane, the Sec machinery does so in an unfolded state (1, 2). Also operating within the eukaryotic cells, the guided entry of tail-anchored (GET) machinery delivers tail-anchored proteins to the endoplasmic reticulum membrane for membrane insertion by a post-translational mechanism (3). A very different translocase called the twin arginine translocation (Tat) machinery functions to translocate folded proteins across the membrane (4, 5). The Tat pathway can translocate proteins across the cytoplasmic membrane in bacterial and archaeal cells and across the thylakoid membrane of chloroplasts.This review will focus on the YidC/Oxa1/Alb3 family of proteins that operates in bacteria and certain eukaryotic organelles to facilitate membrane protein insertion. We will discuss the distribution and function of these insertases and highlight the recent structural work on these novel proteins, which provides insight into how these proteins catalyze membrane protein insertion and protein assembly at a molecular level.

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“…In cooperation with the Sec translocase, YidC assists in the membrane insertion of CyoA (11,12), NuoK (13), and F 0 a and F 0 b subunits of F 1 F 0 ATPase (14), and the translocation of the periplasmic loop 1 and loop 2 of TatC (15). It also acts as a chaperone in the folding of lactose permease LacY and MalF (16,17).…”

mentioning

confidence: 99%

Role of the Cytosolic Loop C2 and the C Terminus of YidC in Ribosome Binding and Insertion Activity

Geng

Kedrov

Caumanns

et al. 2015

Journal of Biological Chemistry

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YidC Protein, a Molecular Chaperone for LacY Protein Folding via the SecYEG Protein Machinery

Cited by 43 publications

References 76 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

YidC/Alb3/Oxa1 Family of Insertases

Role of the Cytosolic Loop C2 and the C Terminus of YidC in Ribosome Binding and Insertion Activity

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