Gene Symbol: surA
Description: peptidyl-prolyl cis-trans isomerase (PPIase)
Alias: ECK0054, JW0052
Species: Escherichia coli str. K-12 substr. MG1655
Products:     surA

Top Publications

  1. Bitto E, McKay D. The periplasmic molecular chaperone protein SurA binds a peptide motif that is characteristic of integral outer membrane proteins. J Biol Chem. 2003;278:49316-22 pubmed
    The Escherichia coli SurA protein is a periplasmic molecular chaperone that facilitates correct folding of outer membrane porins...
  2. Alcock F, Grossmann J, Gentle I, Likic V, Lithgow T, Tokatlidis K. Conserved substrate binding by chaperones in the bacterial periplasm and the mitochondrial intermembrane space. Biochem J. 2008;409:377-87 pubmed
    ..The mitochondrial TIM (translocase of the mitochondrial inner membrane) 10 complex and the periplasmic chaperone SurA were examined in terms of evolutionary relation, structural similarity, substrate binding specificity and their ..
  3. Behrens S. Periplasmic chaperones--new structural and functional insights. Structure. 2002;10:1469-71 pubmed
    ..New intriguing functional insights are provided by the solved crystal structure of the periplasmic chaperone SurA.
  4. Lazar S, Kolter R. SurA assists the folding of Escherichia coli outer membrane proteins. J Bacteriol. 1996;178:1770-3 pubmed
    ..b>SurA, a periplasmic protein of Escherichia coli, has sequence similarity with the prolyl isomerase parvulin...
  5. Ades S, Connolly L, Alba B, Gross C. The Escherichia coli sigma(E)-dependent extracytoplasmic stress response is controlled by the regulated proteolysis of an anti-sigma factor. Genes Dev. 1999;13:2449-61 pubmed
    ..We present evidence that the putative inner membrane serine protease, DegS, is responsible for this regulated degradation of RseA. ..
  6. Hennecke G, Nolte J, Volkmer Engert R, Schneider Mergener J, Behrens S. The periplasmic chaperone SurA exploits two features characteristic of integral outer membrane proteins for selective substrate recognition. J Biol Chem. 2005;280:23540-8 pubmed
    The Escherichia coli periplasmic chaperone and peptidyl-prolyl isomerase (PPIase) SurA facilitates the maturation of outer membrane porins...
  7. Ureta A, Endres R, Wingreen N, Silhavy T. Kinetic analysis of the assembly of the outer membrane protein LamB in Escherichia coli mutants each lacking a secretion or targeting factor in a different cellular compartment. J Bacteriol. 2007;189:446-54 pubmed
    ..Moreover, we found that surA mutants are qualitatively indistinguishable from yfgL mutants, suggesting that the products of both of these genes ..
  8. Rouvi re P, de las Pe as A, Mecsas J, Lu C, Rudd K, Gross C. rpoE, the gene encoding the second heat-shock sigma factor, sigma E, in Escherichia coli. EMBO J. 1995;14:1032-42 pubmed
    ..Based upon homology arguments, we suggest that a gene encoding a negative regulator of sigma E activity is located immediately downstream of rpoE and may function as the target of the E sigma E inducing signal...
  9. Missiakas D, Betton J, Raina S. New components of protein folding in extracytoplasmic compartments of Escherichia coli SurA, FkpA and Skp/OmpH. Mol Microbiol. 1996;21:871-84 pubmed
    ..Using multicopy libraries, we cloned two genes, surA and fkpA, that decreased the sigma E-dependent response constitutively induced by misfolded proteins...

More Information


  1. Vuong P, Bennion D, Mantei J, Frost D, Misra R. Analysis of YfgL and YaeT interactions through bioinformatics, mutagenesis, and biochemistry. J Bacteriol. 2008;190:1507-17 pubmed publisher
    ..The five YfgL mutants defective in YaeT associations and the yfgL background were used to show that SurA binds to YaeT (or another complex member) without going through YfgL.
  2. Schleiff E, Soll J. Membrane protein insertion: mixing eukaryotic and prokaryotic concepts. EMBO Rep. 2005;6:1023-7 pubmed
    ..This review focuses on recent advances in the elucidation of the evolutionarily conserved concepts that underlie the translocation and insertion of beta-barrel membrane proteins. ..
  3. Dartigalongue C, Raina S. A new heat-shock gene, ppiD, encodes a peptidyl-prolyl isomerase required for folding of outer membrane proteins in Escherichia coli. EMBO J. 1998;17:3968-80 pubmed
    ..The gene encoding PpiD was isolated as a multicopy suppressor of surA, a mutation which severely impairs the folding of outer membrane proteins (OMPs)...
  4. Behrens S, Maier R, de Cock H, Schmid F, Gross C. The SurA periplasmic PPIase lacking its parvulin domains functions in vivo and has chaperone activity. EMBO J. 2001;20:285-94 pubmed
    The Escherichia coli periplasmic peptidyl-prolyl isomerase (PPIase) SurA is involved in the maturation of outer membrane porins. SurA consists of a substantial N-terminal region, two iterative parvulin-like domains and a C-terminal tail...
  5. Onufryk C, Crouch M, Fang F, Gross C. Characterization of six lipoproteins in the sigmaE regulon. J Bacteriol. 2005;187:4552-61 pubmed
    ..Both deltayraP and deltanlpB are synthetically lethal with surA::Cm, which encodes a periplasmic chaperone and PPIase, suggesting that NlpB and YraP play roles in a periplasmic ..
  6. Bitto E, McKay D. Crystallographic structure of SurA, a molecular chaperone that facilitates folding of outer membrane porins. Structure. 2002;10:1489-98 pubmed
    The SurA protein facilitates correct folding of outer membrane proteins in gram-negative bacteria...
  7. Sklar J, Wu T, Kahne D, Silhavy T. Defining the roles of the periplasmic chaperones SurA, Skp, and DegP in Escherichia coli. Genes Dev. 2007;21:2473-84 pubmed
    ..membrane through an unknown mechanism that requires the outer membrane YaeT complex and the periplasmic chaperones SurA, DegP, and Skp...
  8. Rouviere P, Gross C. SurA, a periplasmic protein with peptidyl-prolyl isomerase activity, participates in the assembly of outer membrane porins. Genes Dev. 1996;10:3170-82 pubmed
    ..We present evidence that SurA, a periplasmic protein with peptidyl-prolyl isomerase activity, is involved in the maturation and assembly of LamB...
  9. Ma H, Buer J, Zeng A. Hierarchical structure and modules in the Escherichia coli transcriptional regulatory network revealed by a new top-down approach. BMC Bioinformatics. 2004;5:199 pubmed
    ..coli. ..
  10. Justice S, Lauer S, Hultgren S, Hunstad D. Maturation of intracellular Escherichia coli communities requires SurA. Infect Immun. 2006;74:4793-800 pubmed
    ..In this study, we investigated the role of SurA in the UPEC pathogenic cascade...
  11. Castanie Cornet M, Cam K, Jacq A. RcsF is an outer membrane lipoprotein involved in the RcsCDB phosphorelay signaling pathway in Escherichia coli. J Bacteriol. 2006;188:4264-70 pubmed
    ..We also report that a null mutation in surA, a gene required for correct folding of periplasmic proteins, activates the Rcs pathway through RcsF...
  12. Muller M, Koch H, Beck K, Schafer U. Protein traffic in bacteria: multiple routes from the ribosome to and across the membrane. Prog Nucleic Acid Res Mol Biol. 2001;66:107-57 pubmed
    ..These folding processes require distinct molecular chaperones of the periplasm, such as Skp, SurA, and PpiD.
  13. Gatsos X, Perry A, Anwari K, Dolezal P, Wolynec P, Likic V, et al. Protein secretion and outer membrane assembly in Alphaproteobacteria. FEMS Microbiol Rev. 2008;32:995-1009 pubmed publisher
    ..g. Skp, YfgL and NlpB), other proteins are conserved but are missing characteristic domains (e.g. SurA)...
  14. Sauri A, Soprova Z, Wickström D, de Gier J, van der Schors R, Smit A, et al. The Bam (Omp85) complex is involved in secretion of the autotransporter haemoglobin protease. Microbiology. 2009;155:3982-91 pubmed publisher
    ..The intermediate was copurified with the periplasmic chaperone SurA and subunits of the Bam (Omp85) complex that catalyse the insertion and assembly of outer-membrane proteins...
  15. O Reilly E, Kreuzer K. Isolation of SOS constitutive mutants of Escherichia coli. J Bacteriol. 2004;186:7149-60 pubmed
    ..This study also provides a quantitative comparison of the extent of SOS expression caused by inactivation of many different genes in a common genetic background. ..
  16. Roa B, Connolly D, Winkler M. Overlap between pdxA and ksgA in the complex pdxA-ksgA-apaG-apaH operon of Escherichia coli K-12. J Bacteriol. 1989;171:4767-77 pubmed
    ..The results are also considered in terms of ksgA expression. ..
  17. Workman P, Heide K, Giuliano N, Lee N, Mar J, Vuong P, et al. Genetic, biochemical, and molecular characterization of the polypeptide transport-associated domain of Escherichia coli BamA. J Bacteriol. 2012;194:3512-21 pubmed publisher
    ..A18S) background, OMP biogenesis improved dramatically, and this correlated with improved BamA folding, BamA-SurA interactions, and LptD (lipopolysaccharide transporter) biogenesis...
  18. Xu X, Wang S, Hu Y, McKay D. The periplasmic bacterial molecular chaperone SurA adapts its structure to bind peptides in different conformations to assert a sequence preference for aromatic residues. J Mol Biol. 2007;373:367-81 pubmed
    The periplasmic molecular chaperone protein SurA facilitates correct folding and maturation of outer membrane proteins in Gram-negative bacteria. It preferentially binds peptides that have a high fraction of aromatic amino acids...
  19. Webb H, Ruddock L, Marchant R, Jonas K, Klappa P. Interaction of the periplasmic peptidylprolyl cis-trans isomerase SurA with model peptides. The N-terminal region of SurA id essential and sufficient for peptide binding. J Biol Chem. 2001;276:45622-7 pubmed
    ..To characterize the interaction between model peptides and the periplasmic peptidylprolyl cis-trans isomerase SurA from E...
  20. Tormo A, Almiron M, Kolter R. surA, an Escherichia coli gene essential for survival in stationary phase. J Bacteriol. 1990;172:4339-47 pubmed
    ..Cells containing suppressing mutations then grew in the same culture to 10(8) cells per ml, taking over the population. The implications of these observations to our understanding of stationary-phase mutagenesis are discussed. ..
  21. Struve C, Forestier C, Krogfelt K. Application of a novel multi-screening signature-tagged mutagenesis assay for identification of Klebsiella pneumoniae genes essential in colonization and infection. Microbiology. 2003;149:167-76 pubmed
    ..Transposon insertion sites in attenuated mutants were, among others, in genes encoding well-known K. pneumoniae virulence factors such as lipopolysaccharide and capsule, as well as in genes of unknown function...
  22. Vulic M, Kolter R. Alcohol-induced delay of viability loss in stationary-phase cultures of Escherichia coli. J Bacteriol. 2002;184:2898-905 pubmed
  23. Cook G, Membrillo Hernandez J, Poole R. Transcriptional regulation of the cydDC operon, encoding a heterodimeric ABC transporter required for assembly of cytochromes c and bd in Escherichia coli K-12: regulation by oxygen and alternative electron acceptors. J Bacteriol. 1997;179:6525-30 pubmed
    ..Aerobic expression was independent of ArcA and Fnr, but induction of cydDC by nitrate and nitrite was dependent on NarL and Fnr...
  24. Stymest K, Klappa P. The periplasmic peptidyl prolyl cis-trans isomerases PpiD and SurA have partially overlapping substrate specificities. FEBS J. 2008;275:3470-9 pubmed publisher
    ..In the periplasmic space of Escherichia coli and other Gram-negative bacteria, two PPIases, SurA and PpiD, have been identified, which show high sequence similarity to the catalytic domain of the small PPIase ..
  25. Schlapschy M, Grimm S, Skerra A. A system for concomitant overexpression of four periplasmic folding catalysts to improve secretory protein production in Escherichia coli. Protein Eng Des Sel. 2006;19:385-90 pubmed
    ..isomerization of disulfide bridges and the peptidyl-prolyl cis/trans-isomerases with chaperone activity, FkpA and SurA. pTUM4 carries a p15a origin of replication and a chloramphenicol resistance gene and, thus, it is compatible with ..
  26. Merz F, Hoffmann A, Rutkowska A, Zachmann Brand B, Bukau B, Deuerling E. The C-terminal domain of Escherichia coli trigger factor represents the central module of its chaperone activity. J Biol Chem. 2006;281:31963-71 pubmed
    ..Intriguingly, a structurally similar module is found in the periplasmic chaperone SurA and in MPN555, a protein of unknown function...
  27. Werner J, Misra R. YaeT (Omp85) affects the assembly of lipid-dependent and lipid-independent outer membrane proteins of Escherichia coli. Mol Microbiol. 2005;57:1450-9 pubmed
    ..Interestingly, assemblies of the two distinct groups of OMPs that follow either SurA- and lipopolysaccharide-dependent (OmpF/C) or -independent (TolC) folding pathways were affected, suggesting that ..
  28. Ricci D, Schwalm J, Gonzales Cope M, Silhavy T. The activity and specificity of the outer membrane protein chaperone SurA are modulated by a proline isomerase domain. MBio. 2013;4: pubmed publisher
    b>SurA is a component of the periplasmic chaperone network that plays a central role in biogenesis of integral outer membrane ?-barrel proteins (OMPs) in Escherichia coli...
  29. Maurer L, Yohannes E, Bondurant S, Radmacher M, Slonczewski J. pH regulates genes for flagellar motility, catabolism, and oxidative stress in Escherichia coli K-12. J Bacteriol. 2005;187:304-19 pubmed
  30. Cuny C, Dukan L, Fraysse L, Ballesteros M, Dukan S. Investigation of the first events leading to loss of culturability during Escherichia coli starvation: future nonculturable bacteria form a subpopulation. J Bacteriol. 2005;187:2244-8 pubmed
    ..Based on these results, we suggest that these physiological differences reflect uncharacterized bacterial modifications which do not directly involve defenses against ROS. ..
  31. Denoncin K, Vertommen D, Paek E, Collet J. The protein-disulfide isomerase DsbC cooperates with SurA and DsbA in the assembly of the essential ?-barrel protein LptD. J Biol Chem. 2010;285:29425-33 pubmed publisher
    ..Two partially redundant chaperones, SurA and Skp, are considered to transport the bulk mass of ?-barrel proteins...
  32. Werner J, Augustus A, Misra R. Assembly of TolC, a structurally unique and multifunctional outer membrane protein of Escherichia coli K-12. J Bacteriol. 2003;185:6540-7 pubmed
    ..None of the assembly steps of TolC is affected by known folding factors, such as SurA, Skp, and lipopolysaccharide, which have profound effects on the assembly of other model trimeric outer membrane ..
  33. Rizzitello A, Harper J, Silhavy T. Genetic evidence for parallel pathways of chaperone activity in the periplasm of Escherichia coli. J Bacteriol. 2001;183:6794-800 pubmed publisher
    ..Using depletion analysis, we directly demonstrated that null mutations in skp and surA, as well as in degP and surA, result in synthetic phenotypes, suggesting that Skp, SurA, and DegP are functionally ..
  34. Rudd K, Sofia H, Koonin E, Plunkett G, Lazar S, Rouviere P. A new family of peptidyl-prolyl isomerases. Trends Biochem Sci. 1995;20:12-4 pubmed
  35. Hansen S, Lewis K, Vulic M. Role of global regulators and nucleotide metabolism in antibiotic tolerance in Escherichia coli. Antimicrob Agents Chemother. 2008;52:2718-26 pubmed publisher
    ..The genes affected in these strains were dnaJ and dnaK (chaperones), apaH (diadenosine tetraphosphatase), surA (peptidyl-prolyl cis-trans isomerase), fis and hns (global regulators), hnr (response regulator of RpoS), dksA (..
  36. Vertommen D, Ruiz N, Leverrier P, Silhavy T, Collet J. Characterization of the role of the Escherichia coli periplasmic chaperone SurA using differential proteomics. Proteomics. 2009;9:2432-43 pubmed publisher
    Little is known on how beta-barrel proteins are assembled in the outer membrane (OM) of Gram-negative bacteria. SurA has been proposed to be the primary chaperone escorting the bulk mass of OM proteins across the periplasm...
  37. Pease A, Roa B, Luo W, Winkler M. Positive growth rate-dependent regulation of the pdxA, ksgA, and pdxB genes of Escherichia coli K-12. J Bacteriol. 2002;184:1359-69 pubmed
    ..Amounts of the pdxB-specific transcript remained unchanged during amino acid starvation in wild-type and relA mutant strains. ..
  38. Matsuyama S, Tokuda H. [Transport of outer membrane proteins]. Tanpakushitsu Kakusan Koso. 2004;49:965-6 pubmed
  39. Han M, Lee S. The Escherichia coli proteome: past, present, and future prospects. Microbiol Mol Biol Rev. 2006;70:362-439 pubmed
    ..Here, we review the past development and current status of E. coli proteome research in terms of its biological, biotechnological, and methodological significance and suggest future prospects. ..
  40. Palomino C, Marín E, Fernández L. The fimbrial usher FimD follows the SurA-BamB pathway for its assembly in the outer membrane of Escherichia coli. J Bacteriol. 2011;193:5222-30 pubmed publisher
    ..Here, we investigate the role of periplasmic chaperones (SurA, Skp, DegP, and FkpA) and individual components of the ?-barrel assembly machinery (BAM) complex (BamA, BamB, BamC, ..
  41. Wiedenmann A, Dimroth P, von Ballmoos C. Functional asymmetry of the F(0) motor in bacterial ATP synthases. Mol Microbiol. 2009;72:479-90 pubmed publisher
    ..5 were required for ATP synthesis in vitro. This discrepancy is discussed with respect to the hypothesis that during respiration lateral proton diffusion could lead to significant acidification at the membrane surface...
  42. Lazar S, Almiron M, Tormo A, Kolter R. Role of the Escherichia coli SurA protein in stationary-phase survival. J Bacteriol. 1998;180:5704-11 pubmed
    b>SurA is a periplasmic peptidyl-prolyl isomerase required for the efficient folding of extracytoplasmic proteins...
  43. Zoldak G, Schmid F. Cooperation of the prolyl isomerase and chaperone activities of the protein folding catalyst SlyD. J Mol Biol. 2011;406:176-94 pubmed publisher
    ..Protein molecules that left the prolyl isomerase site with an incorrect prolyl isomer can rapidly be re-bound by the chaperone domain because the association rate is very high as well. ..
  44. Mogensen J, Kleinschmidt J, Schmidt M, Otzen D. Misfolding of a bacterial autotransporter. Protein Sci. 2005;14:2814-27 pubmed
    ..We conclude that it is the exposure to the unique spatial arrangement of the bacterial cell that leads to proper refolding of the beta-domain. ..
  45. Justice S, Hunstad D, Harper J, Duguay A, Pinkner J, Bann J, et al. Periplasmic peptidyl prolyl cis-trans isomerases are not essential for viability, but SurA is required for pilus biogenesis in Escherichia coli. J Bacteriol. 2005;187:7680-6 pubmed
    In Escherichia coli, FkpA, PpiA, PpiD, and SurA are the four known periplasmic cis-trans prolyl isomerases...
  46. Bothmann H, Pluckthun A. The periplasmic Escherichia coli peptidylprolyl cis,trans-isomerase FkpA. I. Increased functional expression of antibody fragments with and without cis-prolines. J Biol Chem. 2000;275:17100-5 pubmed
    ..In contrast, the coexpression of the periplasmic PPIases PpiA and SurA showed no increase in the functional scFv fragment level in the periplasm or displayed on phage...
  47. Miot M, Betton J. Protein quality control in the bacterial periplasm. Microb Cell Fact. 2004;3:4 pubmed
    ..This article summarizes the general principles which control protein folding in the bacterial periplasm by focusing on the periplasmic maltose-binding protein. ..
  48. Behrens Kneip S. The role of SurA factor in outer membrane protein transport and virulence. Int J Med Microbiol. 2010;300:421-8 pubmed publisher
    The Escherichia coli periplasmic chaperone and peptidyl-prolyl isomerase (PPIase) SurA is a major factor in the biogenesis of ?-barrel outer membrane proteins (OMPs) and as such plays an integral role in cell envelope homeostasis and cell ..
  49. Soltes G, Schwalm J, Ricci D, Silhavy T. The Activity of Escherichia coli Chaperone SurA Is Regulated by Conformational Changes Involving a Parvulin Domain. J Bacteriol. 2016;198:921-9 pubmed publisher
    The periplasmic chaperone SurA is critical for the biogenesis of outer membrane proteins (OMPs) and, thus, the maintenance of membrane integrity in Escherichia coli...
  50. Smith L, Gomez M, Shatalin K, Lee H, Neyfakh A. Monitoring of gene knockouts: genome-wide profiling of conditionally essential genes. Genome Biol. 2007;8:R87 pubmed
    ..Our findings suggest that MGK can serve as a robust tool in functional genomics studies. ..
  51. Zhong M, Ferrell B, Lu W, Chai Q, Wei Y. Insights into the function and structural flexibility of the periplasmic molecular chaperone SurA. J Bacteriol. 2013;195:1061-7 pubmed publisher
    b>SurA is the primary periplasmic molecular chaperone that facilitates the folding and assembling of outer membrane proteins (OMPs) in Gram-negative bacteria...
  52. Niba E, Naka Y, Nagase M, Mori H, Kitakawa M. A genome-wide approach to identify the genes involved in biofilm formation in E. coli. DNA Res. 2007;14:237-46 pubmed publisher
    ..of the nine mutants of function-unknown genes indicated that some of them, such as yfgA that genetically interacts with a periplasmic chaperone gene surA together with yciB and yciM, might be required for the integrity of outer membrane.
  53. Charlson E, Werner J, Misra R. Differential effects of yfgL mutation on Escherichia coli outer membrane proteins and lipopolysaccharide. J Bacteriol. 2006;188:7186-94 pubmed
    ..The results support the hypothesis that TolC and major outer membrane proteins compete for the YaeT/YfiO complex, since mutations that adversely affect synthesis or assembly of major outer membrane proteins lead to elevated TolC levels. ..