The DOI matches its Crossref record; 1 of the 1 references it cites were found in a registry or an index.
The outer membrane lipoprotein NlpI nucleates hydrolases within peptidoglycan multi-enzyme complexes in Escherichia coli
Open accessPreprint — published as 10.15252/embj.2019102246
Abstract
The peptidoglycan (PG) sacculus provides bacteria with the mechanical strength to maintain cell shape and resist osmotic stress. Enlargement of the mesh-like sacculus requires the combined activity of PG synthases and hydrolases. In Escherichia coli , the activity of the two bifunctional PG synthases is driven by lipoproteins anchored in the outer membrane. However, the regulation of PG hydrolases is less well understood, with only regulators for PG amidases having been described. Here, we identify the lipoprotein NlpI as a general adaptor protein for PG hydrolases. NlpI binds to different classes of hydrolases and can specifically form multimeric complexes with various PG endopeptidases. In addition, NlpI seems to contribute both to PG elongation and cell division biosynthetic complexes based on its localization and genetic interactions. In line with such a role, we reconstitute PG multi-enzyme complexes containing NlpI, the PG synthesis regulator LpoA, its cognate bifunctional synthase, PBP1A, and different endopeptidases. Our results indicate that PG regulators and adaptors are part of PG biosynthetic multi-enzyme complexes, regulating and potentially coordinating the spatiotemporal action of PG synthases and hydrolases. Significance: The activity of PG hydrolases may cause lysis of the bacterial cell if left unregulated. Hence, the cell must have ways of regulating and coordinating their activities. Our current understanding of how this occurs is incomplete. In this work, we present the outer membrane (OM) anchored lipoprotein, NlpI, as a scaffold of peptidoglycan hydrolases. We propose that NlpI facilitates the formation of multi-enzyme complexes and that, along with other regulators, it coordinates a safe enlargement and separation of the PG layer in E. coli .
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Global quantification of mammalian gene expression control
Schwanhäusser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W., & Selbach, M. (2011) · Nature · doi:10.1038/nature10098 · Cited by 6,566 · cited 1×
“Label free quantification was selected using iBAQ (calculated as the sum of the intensities of the identified peptides and divided by the number of observable peptides of a protein) (Schwanhausser et al., 2011), with the log fit function enabled.”
Method
Flagged first, then by citations
Research works printed but not linked: 65
- 10.1073/pnas.44.6.590 · DOI
- 10.1038/msb4100050 · DOI · Paper page
- 10.1111/j.1365-2958.2012.08103.x · DOI
- 2018, Pervasive protein thermal stability variation during the cell cycle, Cell, 173, 1495, 10.1016/j.cell.2018.03.053 · DOI
- 1995, The periplasmic space and the periplasm in Gram-positive and Gram-negative bacteria, ASM News, 61, 125
- 10.1002/(SICI)1521-1878(199911)21:11<932::AID-BIES5>3.0.CO;2-N · DOI
- 10.1074/jbc.M604083200 · DOI
- 10.1007/s00249-009-0418-0 · DOI
- 10.1016/0378-1119(95)00193-A · DOI
- Chodisetti, P. K. & Reddy, M . (2019). Peptidoglycan hydrolase of an unusual cross-link cleavage specificity contributes to bacterial cell wall synthesis. Proc Natl Acad Sci U S A. · DOI
- 2006, Ligand binding by TPR domains, Protein Science: A Publication of the Protein Society, 15, 1193, 10.1110/ps.062092506 · DOI
- 2008, MaxQuant enables high peptide identification rates, individualized p, p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol, 26, 1367
- 10.1093/emboj/17.5.1192 · DOI
- 10.1073/pnas.120163297 · DOI
- 10.1046/j.1365-2958.2003.03316.x · DOI
- 10.1016/j.mib.2017.01.007 · DOI
- 10.1128/IAI.00012-14 · DOI
- 10.1111/mmi.13908 · DOI
- 10.1038/nprot.2015.101 · DOI
- 10.1016/0003-2697(88)90468-X · DOI
- 10.7554/eLife.07118 · DOI
- Höltje, J.-V. (1993). “Three for one” — a Simple Growth Mechanism that Guarantees a Precise Copy of the Thin, Rod-Shaped Murein Sacculus of Escherichia coli . In Bacterial Growth and Lysis: Metabolism and Structure of the Bacterial Sacculus, pp. 419–426. Edited by M. A. de Pedro , J. V. Höltje & W. Löffelhardt . Boston, MA: Springer US.
- 10.1093/bioinformatics/18.suppl_1.S96 · DOI · Paper page
- 1998, Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli, Microbiol Mol Biol Rev, 62, 181, 10.1128/MMBR.62.1.181-203.1998 · DOI · Paper page
- 10.1016/j.str.2014.04.017 · DOI
- 10.1089/adt.2011.0380 · DOI
- 10.1021/bi051533t · DOI
- 2017, A tool named Iris for versatile high-throughput phenotyping in microorganisms, Nat Microbiol, 2, 17014, 10.1038/nmicrobiol.2017.14 · DOI
- 10.1371/journal.pgen.1006934 · DOI
- 10.1016/j.cell.2014.02.033 · DOI
- 10.15252/msb.20188242 · DOI
- 2019, Peptidoglycan remodeling enables Escherichia coli to survive severe outer membrane assembly defect, mBio, 10, e02729
- 10.1038/nrmicro.2016.191 · DOI
- 1999, Identification and characterization of a new lipoprotein, NlpI, in Escherichia coli K-12, J Bacteriol, 181, 4318, 10.1128/JB.181.14.4318-4325.1999 · DOI
- 10.1016/j.cell.2010.11.037 · DOI
- 10.1016/j.mib.2017.01.006 · DOI
- 10.1111/mmi.12304 · DOI
- 10.1093/nar/gkv007 · DOI · Paper page
- 10.1126/science.1255784 · DOI · Paper page
- 10.1016/S0006-3495(00)76713-0 · DOI
- 10.1002/mbo3.244 · DOI
- 10.1101/cshperspect.a000414 · DOI
- 10.1111/mmi.12058 · DOI
- 10.1073/pnas.1507760112 · DOI
- 10.1038/s41467-017-01697-9 · DOI
- 10.1128/IAI.00034-10 · DOI
- 10.1038/srep18190 · DOI
- 2017, NlpD links cell wall remodeling and outer membrane invagination during cytokinesis in Escherichia coli, PLOS Genetics, 13, e1006888, 10.1371/journal.pgen.1006888 · DOI
- 10.1016/j.cell.2010.11.038 · DOI
- 10.1038/nrmicro2677 · DOI
- 10.1038/nrmicro3508 · DOI
- 10.1128/JB.00505-09 · DOI
- 10.1038/emboj.2010.36 · DOI
- 10.1128/MMBR.00022-11 · DOI
- Vischer, N. O. E. , Verheul, J. , Postma, M. , van den Berg van Saparoea, B. , Galli, E. , Natale, P. , Gerdes, K. , Luirink, J. , Vollmer, W. , Vicente, M. & den Blaauwen, T. (2015). Cell age dependent concentration of Escherichia coli divisome proteins analyzed with ImageJ and ObjectJ. Frontiers in Microbiology 6. · DOI
- 10.1074/jbc.274.10.6726 · DOI
- 10.1111/j.1574-6976.2007.00094.x · DOI
- 10.1111/j.1574-6976.2007.00099.x · DOI
- 10.1111/j.1432-1033.2004.04397.x · DOI
- 10.1111/j.1365-2958.2012.08138.x · DOI
- 10.1099/00221287-131-10-2839 · DOI
- 2016, Identification of MltG as a potential terminase for peptidoglycan polymerization in bacteria, Mol Microbiol, 99, 700, 10.1111/mmi.13258 · DOI
- 10.1016/0003-2697(88)90468-X · DOI
- 10.1089/adt.2011.0380 · DOI
- 10.15252/msb.20188242 · DOI
Metadata
- Authors
- Banzhaf, M., Yau, H. C. L., Verheul, J., Lodge, A., Kritikos, G., Mateus, A., Hov, A. K., Stein, F., Wartel, M., Pazos, M., Solovyova, A. S., Savitski, M. M., den Blaauwen, T., Typas, A., & Vollmer, W.
- Affiliations
- European Molecular Biology Laboratory (DE)
- Newcastle University (GB)
- University of Amsterdam (NL)
- Corresponding author
- den Blaauwen, Tanneke
- Typas, Athanasios
- Vollmer, Waldemar
- ORCID
- Venue
- The EMBO Journal
- Publisher
- openRxiv
- Published
- 2019-04-16
- Volume
- 39
- Issue
- 5
- Pages
- e102246-e102246
- ISSN
- 0261-4189 (ISSN-L)
- PMC
- PMC7049810
- OpenAlex
- W3003362316
- Cited by
- 89
- References
- 1
- Citations by year
- 2026: 4 · 2025: 9 · 2024: 12 · 2023: 14 · 2022: 11 · 2021: 21 · 2020: 18
- FWCI
- 9.38
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- other-oa
- Locations
- The EMBO Journal (publishedVersion, other-oa)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- UvA-DARE (University of Amsterdam) (submittedVersion, other-oa)
- HAL (submittedVersion, cc-by)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
- University of Birmingham Research Portal (University of Birmingham) (submittedVersion, cc-by)
- Utrecht University Repository (Utrecht University) (submittedVersion, cc-by)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Funders
- Alexander von Humboldt-Stiftung
- Wellcome Trust (101824/Z/13/Z, 101824)
- European Molecular Biology Laboratory (664726)
- Royal Society (RGS\R1\191041)
- European Commission (664726, HORIZON2020)
- Volkswagen Foundation
- Agence Nationale de la Recherche (10-LABX-62-IBEID, ANR‐10‐LABX‐62‐IBEID, ANR-10, ANR-10-LABX-0062, ANR-10-LABX-62)
- Medical Research Council (MR/N501840/1, MR/N002679/1, 101824/Z/13/Z)
- European Research Council (679980)
- H2020 Marie Skłodowska-Curie Actions (EI3POD, HORIZON2020, 664726)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Immunology and Microbiology › Microbiology › Escherichia coli research studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Biochemical and Structural Characterization
- Keywords
- outer membrane lipoprotein, peptidoglycan hydrolase, multienzyme complex, peptidoglycan biosynthesis, cell division, PBP1a, adaptor proteins, Escherichia coli
- MeSH terms
- Cell Wall, Escherichia coli, Lipoproteins, Multienzyme Complexes, N-Acetylmuramoyl-L-alanine Amidase, Endopeptidases, Peptidoglycan, Escherichia coli Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
