Student or educator? Sign up with your school email and get 6 months of Pro free.
CoChat
Sign Up
Cited by 169

The DOI matches its Crossref record; 4 of the 4 references it cites were found in a registry or an index.

Small Stress Response Proteins in Escherichia coli : Proteins Missed by Classical Proteomic Studies

Open access
Hemm, Matthew R., Paul, Brian J., Miranda-Ríos, Juan, Zhang, Aixia, Soltanzad, Nima, Storz, Gisela·2010·Journal of Bacteriology
DOI 10.1128/jb.00872-09
Open this paper in CoChat — free account

Abstract

Proteins of 50 or fewer amino acids are poorly characterized in all organisms. The corresponding genes are challenging to reliably annotate, and it is difficult to purify and characterize the small protein products. Due to these technical limitations, little is known about the abundance of small proteins, not to mention their biological functions. To begin to characterize these small proteins in Escherichia coli , we assayed their accumulation under a variety of growth conditions and after exposure to stress. We found that many small proteins accumulate under specific growth conditions or are stress induced. For some genes, the observed changes in protein levels were consistent with known transcriptional regulation, such as ArcA activation of the operons encoding yccB and ybgT . However, we also identified novel regulation, such as Zur repression of ykgMO , cyclic AMP response protein (CRP) repression of azuC , and CRP activation of ykgR . The levels of 11 small proteins increase after heat shock, and induction of at least 1 of these, YobF, occurs at a posttranscriptional level. These results show that small proteins are an overlooked subset of stress response proteins in E. coli and provide information that will be valuable for determining the functions of these proteins.

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.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1128/jb.00872-09

Cites

4 of 4 references verified0 citation errors · 0 not checkable

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.

A few free checks a day · papers already verified open instantly · results are public

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

Show all 4 references

Research works printed but not linked: 48

  1. Ades, S. E. 2008. Regulation by destruction: design of the σE envelope stress response. Curr. Opin. Microbiol. 11 : 535-540. · DOI · Paper page
  2. Alix, E., and A. B. Blanc-Potard. 2008. Peptide-assisted degradation of the Salmonella MgtC virulence factor. EMBO J. 27 : 546-557. · DOI
  3. 10.1128/jb.178.6.1556-1564.1996 · DOI
  4. Burkholder, W. F., I. Kurtser, and A. D. Grossman. 2001. Replication initiation proteins regulate a developmental checkpoint in Bacillus subtilis. Cell 104 : 269-279. · DOI · Paper page
  5. Castanie-Cornet, M. P., and J. W. Foster. 2001. Escherichia coli acid resistance: cAMP receptor protein and a 20 bp cis-acting sequence control pH and stationary phase expression of the gadA and gadBC glutamate decarboxylase genes. Microbiology 147 : 709-715. · DOI · Paper page
  6. Chen, S., E. A. Lesnik, T. A. Hall, R. Sampath, R. H. Griffey, D. J. Ecker, and L. B. Blyn. 2002. A bioinformatics based approach to discover small RNA genes in the Escherichia coli genome. Biosystems 65 : 157-177. · DOI · Paper page
  7. 10.1016/0378-1119(95)00193-A · DOI · Paper page
  8. 10.1128/jb.172.11.6333-6338.1990 · DOI · Paper page
  9. Dassa, J., H. Fsihi, C. Marck, M. Dion, M. Kieffer-Bontemps, and P. L. Boquet. 1991. A new oxygen-regulated operon in Escherichia coli comprises the genes for a putative third cytochrome oxidase and for pH 2.5 acid phosphatase (appA). Mol. Gen. Genet. 229 : 341-352. · DOI
  10. 10.1128/JB.01157-08 · DOI · Paper page
  11. Fountoulakis, M., M. F. Takács, P. Berndt, H. Langen, and B. Takács. 1999. Enrichment of low abundance proteins of Escherichia coli by hydroxyapatite chromatography. Electrophoresis 20 : 2181-2195. · doi:10.1002/(sici)1522-2683(19990801)20:11<2181::aid-elps2181>3.0.co;2-q
  12. Fozo, E. M., M. Kawano, Y. Kaya, K. Jones, K. E. Rudd, and G. Storz. 2008. Repression of small toxic protein synthesis by the Sib and OhsC small RNAs. Mol. Microbiol. 70 : 1076-1093. · DOI · Paper page
  13. 10.1128/JB.00802-09 · DOI
  14. Galindo, M. I., J. I. Pueyo, S. Fouix, S. A. Bishop, and J. P. Couso. 2007. Peptides encoded by short ORFs control development and define a new eukaryotic gene family. PLoS Biol. 5 : 1052-1062.
  15. Gautier, R., D. Douguet, B. Antonny, and G. Drin. 2008. HELIQUEST: a web server to screen sequences with specific α-helical properties. Bioinformatics 24 : 2101-2102. · DOI · Paper page
  16. 10.1128/JB.186.11.3516-3524.2004 · DOI · Paper page
  17. Grainger, D. C., D. Hurd, M. Harrison, J. Holdstock, and S. J. Busby. 2005. Studies of the distribution of Escherichia coli cAMP-receptor protein and RNA polymerase along the E. coli chromosome. Proc. Natl. Acad. Sci. U. S. A. 102 : 17693-17698. · DOI · Paper page
  18. 10.1128/MMBR.00007-08 · DOI · Paper page
  19. 10.1128/jb.177.14.4121-4130.1995 · DOI · Paper page
  20. 10.1128/MMBR.00036-05 · DOI · Paper page
  21. Hemm, M. R., B. J. Paul, T. D. Schneider, G. Storz, and K. E. Rudd. 2008. Small membrane proteins found by comparative genomics and ribosome binding site models. Mol. Microbiol. 70 : 1487-1501. · DOI · Paper page
  22. 10.1128/JB.00873-09 · DOI
  23. Huerta, A. M., and J. Collado-Vides. 2003. σ70 promoters in Escherichia coli: specific transcription in dense regions of overlapping promoter-like signals. J. Mol. Biol. 333 : 261-278. · DOI · Paper page
  24. Laskowska, E., A. Wawrzynów, and A. Taylor. 1996. IbpA and IbpB, the new heat-shock proteins, bind to endogenous Escherichia coli proteins aggregated intracellularly by heat shock. Biochimie 78 : 117-122. · DOI
  25. Law, E. C., N. J. Savery, and S. J. Busby. 1999. Interactions between the Escherichia coli cAMP receptor protein and the C-terminal domain of the alpha subunit of RNA polymerase at class I promoters. Biochem. J. 337 : 415-423. · doi:10.1042/bj3370415
  26. Lawson, C. L., D. Swigon, K. S. Murakami, S. A. Darst, H. M. Berman, and R. H. Ebright. 2004. Catabolite activator protein: DNA binding and transcription activation. Curr. Opin. Struct. Biol. 14 : 10-20. · DOI · Paper page
  27. Lies, M., and M. R. Maurizi. 2008. Turnover of endogenous SsrA-tagged proteins mediated by ATP-dependent proteases in Escherichia coli. J. Biol. Chem. 283 : 22918-22929. · DOI
  28. Link, A. J., K. Robison, and G. M. Church. 1997. Comparing the predicted and observed properties of proteins encoded in the genome of Escherichia coli K-12. Electrophoresis 18 : 1259-1313. · DOI · Paper page
  29. Ma, Z., S. Gong, H. Richard, D. L. Tucker, T. Conway, and J. W. Foster. 2003. GadE (YhiE) activates glutamate decarboxylase-dependent acid resistance in Escherichia coli K-12. Mol. Microbiol. 49 : 1309-1320. · doi:10.1046/j.1365-2958.2003.03633.x
  30. Mandin, P., and S. Gottesman. 2009. A genetic approach for finding small RNAs regulators of genes of interest identifies RybC as regulating the DpiA/DpiB two-component system. Mol. Microbiol. 72 : 551-565. · DOI
  31. Matuszewska, M., D. Kuczyńska-Wiśnik, E. Laskowska, and K. Liberek. 2005. The small heat shock protein IbpA of Escherichia coli cooperates with IbpB in stabilization of thermally aggregated proteins in a disaggregation competent state. J. Biol. Chem. 280 : 12292-12298. · DOI
  32. Narberhaus, F., T. Waldminghaus, and S. Chowdhury. 2006. RNA thermometers. FEMS Microbiol. Rev. 30 : 3-16. · DOI · Paper page
  33. Panina, E. M., A. A. Mironov, and M. S. Gelfand. 2003. Comparative genomics of bacterial zinc regulons: enhanced ion transport, pathogenesis, and rearrangement of ribosomal proteins. Proc. Natl. Acad. Sci. U. S. A. 100 : 9912-9917. · DOI · Paper page
  34. Rhee, K. Y., B. S. Parekh, and G. W. Hatfield. 1996. Leucine-responsive regulatory protein-DNA interactions in the leader region of the ilvGMEDA operon of Escherichia coli. J. Biol. Chem. 271 : 26499-26507. · DOI
  35. Rokney, A., O. Kobiler, A. Amir, D. L. Court, J. Stavans, S. Adhya, and A. B. Oppenheim. 2008. Host responses influence on the induction of lambda prophage. Mol. Microbiol. 68 : 29-36. · DOI
  36. Rowland, S. L., W. F. Burkholder, K. A. Cunningham, M. W. Maciejewski, A. D. Grossman, and G. F. King. 2004. Structure and mechanism of action of Sda, an inhibitor of the histidine kinases that regulate initiation of sporulation in Bacillus subtilis. Mol. Cell 13 : 689-701. · DOI
  37. Rudd, K. E., I. Humphery-Smith, V. C. Wasinger, and A. Bairoch. 1998. Low molecular weight proteins: a challenge for post-genomic research. Electrophoresis 19 : 536-544. · DOI
  38. 10.1128/JB.187.5.1792-1798.2005 · DOI · Paper page
  39. 10.1128/jb.178.6.1742-1749.1996 · doi:10.1128/jb.178.6.1742-1749.1996
  40. 10.1128/jb.144.1.279-290.1980 · doi:10.1128/jb.144.1.279-290.1980
  41. Tjaden, B., S. S. Goodwin, J. A. Opdyke, M. Guillier, D. X. Fu, S. Gottesman, and G. Storz. 2006. Target prediction for small, noncoding RNAs in bacteria. Nucleic Acids Res. 34 : 2791-2802. · DOI · Paper page
  42. Wadler, C. S., and C. K. Vanderpool. 2007. A dual function for a bacterial small RNA: SgrS performs base pairing-dependent regulation and encodes a functional polypeptide. Proc. Natl. Acad. Sci. U. S. A. 104 : 20454-20459. · DOI · Paper page
  43. Waldminghaus, T., A. Fippinger, J. Alfsmann, and F. Narberhaus. 2005. RNA thermometers are common in α- and γ-proteobacteria. Biol. Chem. 386 : 1279-1286. · DOI
  44. Waldminghaus, T., N. Heidrich, S. Brantl, and F. Narberhaus. 2007. FourU: a novel type of RNA thermometer in Salmonella. Mol. Microbiol. 65 : 413-424. · DOI
  45. Wawrzynow, A., J. L. Theibert, C. Murphy, I. Jona, A. Martonosi, and J. H. Collins. 1992. Sarcolipin, the “proteolipid” of skeletal muscle sarcoplasmic reticulum, is a unique, amphipathic, 31-residue peptide. Arch. Biochem. Biophys. 298 : 620-623. · DOI
  46. Xia, B., H. Ke, and M. Inouye. 2001. Acquirement of cold sensitivity by quadruple deletion of the cspA family and its suppression by PNPase S1 domain in Escherichia coli. Mol. Microbiol. 40 : 179-188. · DOI · Paper page
  47. Yamanaka, K., W. Zheng, E. Crooke, Y. H. Wang, and M. Inouye. 2001. CspD, a novel DNA replication inhibitor induced during the stationary phase in Escherichia coli. Mol. Microbiol. 39 : 1572-1584. · doi:10.1046/j.1365-2958.2001.02345.x
  48. Zhang, A., S. Altuvia, A. Tiwari, L. Argaman, R. Hengge-Aronis, and G. Storz. 1998. The OxyS regulatory RNA represses rpoS translation and binds the Hfq (HF-I) protein. EMBO J. 17 : 6061-6068. · DOI · Paper page

Cited by

See all 169

Metadata

Authors
Hemm, M. R., Paul, B. J., Miranda-Ríos, J., Zhang, A., Soltanzad, N., & Storz, G.
Venue
Journal of Bacteriology
Publisher
American Society for Microbiology
Published
2010-01
Volume
192
Issue
1
Pages
46-58
ISSN
  • 0021-9193 (ISSN-L)
  • 1098-5530
DOI
10.1128/jb.00872-09
OpenAlex
W2117725451
Cited by
169
References
4
FWCI
5.35
Type
journal article
Language
en
Open access
green
Licence
journals.asm.org/non-commercial-tdm-license (tdm)

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

How to cite

Cite CoChat for the checks on this page, and the paper for its own findings.

This page
CoChat. (2026). Citation check: Small Stress Response Proteins in Escherichia coli : Proteins Missed by Classical Proteomic Studies. https://app.cochat.ai/papers/10.1128/jb.00872-09
The paper
Hemm, M. R., Paul, B. J., Miranda-Ríos, J., Zhang, A., Soltanzad, N., & Storz, G. (2010). Small Stress Response Proteins in Escherichia coli : Proteins Missed by Classical Proteomic Studies. Journal of Bacteriology. https://doi.org/10.1128/jb.00872-09

Data sources

Bibliographic data: Semantic Scholar, OpenAlex, Crossref.

Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).

Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.