tolA

Summary

Gene Symbol: tolA
Description: membrane anchored protein in TolA-TolQ-TolR complex
Alias: ECK0728, JW0729, cim, excC, lky
Species: Escherichia coli str. K-12 substr. MG1655

Top Publications

  1. Cascales E, Lloubes R, Sturgis J. The TolQ-TolR proteins energize TolA and share homologies with the flagellar motor proteins MotA-MotB. Mol Microbiol. 2001;42:795-807 pubmed
    ..been found to be necessary for the co-precipitation of the outer membrane lipoprotein Pal with the inner membrane TolA protein, indicating that the Tol-Pal system forms a transmembrane link in which TolA is energized...
  2. Lloubes R, Cascales E, Walburger A, Bouveret E, Lazdunski C, Bernadac A, et al. The Tol-Pal proteins of the Escherichia coli cell envelope: an energized system required for outer membrane integrity?. Res Microbiol. 2001;152:523-9 pubmed
    ..These two systems, containing an energized inner membrane protein interacting with outer membrane proteins, share similarities. ..
  3. Cascales E, Gavioli M, Sturgis J, Lloubes R. Proton motive force drives the interaction of the inner membrane TolA and outer membrane pal proteins in Escherichia coli. Mol Microbiol. 2000;38:904-15 pubmed
    The Tol-Pal system of the Escherichia coli envelope is formed from the inner membrane TolQ, TolR and TolA proteins, the periplasmic TolB protein and the outer membrane Pal lipoprotein...
  4. Levengood S, Webster R. Nucleotide sequences of the tolA and tolB genes and localization of their products, components of a multistep translocation system in Escherichia coli. J Bacteriol. 1989;171:6600-9 pubmed
    ..The nucleotide sequence of a 2.8-kilobase fragment containing the tolA and tolB genes was determined...
  5. Meury J, Devilliers G. Impairment of cell division in tolA mutants of Escherichia coli at low and high medium osmolarities. Biol Cell. 1999;91:67-75 pubmed
    Mutations in the tolA gene of Escherichia coli cause the cell to become sensitive to detergents and to some antibiotics, to release periplasmic enzymes and to be resistant to group A colicins; tolA mutations also lead to mucoid phenotype...
  6. Bernadac A, Gavioli M, Lazzaroni J, Raina S, Lloubes R. Escherichia coli tol-pal mutants form outer membrane vesicles. J Bacteriol. 1998;180:4872-8 pubmed
    ..This phenotype was not observed in tolC and rfaD cells in the same conditions. A tolA deletion in three different Escherichia coli strains was shown to lead to elevated amounts of vesicles...
  7. Schendel S, Click E, Webster R, Cramer W. The TolA protein interacts with colicin E1 differently than with other group A colicins. J Bacteriol. 1997;179:3683-90 pubmed
    The 421-residue protein TolA is required for the translocation of group A colicins (colicins E1, E2, E3, A, K, and N) across the cell envelope of Escherichia coli...
  8. Hecht O, Zhang Y, Li C, Penfold C, James R, Moore G. Characterisation of the interaction of colicin A with its co-receptor TolA. FEBS Lett. 2010;584:2249-52 pubmed publisher
    Colicin A enters Escherichia coli cells through interaction with endogenous TolA and TolB proteins. In vitro, binding of the colicin A translocation domain to TolA leads to unfolding of TolA...
  9. Click E, Webster R. Filamentous phage infection: required interactions with the TolA protein. J Bacteriol. 1997;179:6464-71 pubmed
    ..Subsequent translocation of phage DNA requires the chromosomally encoded TolQ, TolR, and TolA proteins, after the pilus presumably has withdrawn, bringing the phage to the bacterial surface...

More Information

Publications64

  1. Journet L, Bouveret E, Rigal A, Lloubes R, Lazdunski C, Benedetti H. Import of colicins across the outer membrane of Escherichia coli involves multiple protein interactions in the periplasm. Mol Microbiol. 2001;42:331-44 pubmed
    ..Colicin A interacts with TolA and TolB via distinct regions of its N-terminal domain. Both interactions are required for colicin translocation...
  2. Dubuisson J, Vianney A, Lazzaroni J. Mutational analysis of the TolA C-terminal domain of Escherichia coli and genetic evidence for an interaction between TolA and TolB. J Bacteriol. 2002;184:4620-5 pubmed
    The Tol proteins are involved in the outer membrane stability of gram-negative bacteria. The C-terminal domain of TolA was mutagenized to identify residues important for its functions...
  3. Levengood S, Beyer W, Webster R. TolA: a membrane protein involved in colicin uptake contains an extended helical region. Proc Natl Acad Sci U S A. 1991;88:5939-43 pubmed
    ..The TolA protein is a 421-amino acid residue integral membrane protein composed of three domains...
  4. Vines E, Marolda C, Balachandran A, Valvano M. Defective O-antigen polymerization in tolA and pal mutants of Escherichia coli in response to extracytoplasmic stress. J Bacteriol. 2005;187:3359-68 pubmed
    We have previously shown that the TolA protein is required for the correct surface expression of the Escherichia coli O7 antigen lipopolysaccharide (LPS). In this work, delta tolA and delta pal mutants of E...
  5. Braun V, Herrmann C. Evolutionary relationship of uptake systems for biopolymers in Escherichia coli: cross-complementation between the TonB-ExbB-ExbD and the TolA-TolQ-TolR proteins. Mol Microbiol. 1993;8:261-8 pubmed
    ..Group B colicins, ferric siderophores and vitamin B12 are taken up via the TonB-ExbB-ExbD, group A colicins via the TolA-TolQ-TolR system...
  6. Germon P, Clavel T, Vianney A, Portalier R, Lazzaroni J. Mutational analysis of the Escherichia coli K-12 TolA N-terminal region and characterization of its TolQ-interacting domain by genetic suppression. J Bacteriol. 1998;180:6433-9 pubmed
    ..They form two complexes in the cell envelope. Transmembrane domains of TolQ, TolR, and TolA interact in the cytoplasmic membrane, while TolB and Pal form a complex near the outer membrane...
  7. Sturgis J. Organisation and evolution of the tol-pal gene cluster. J Mol Microbiol Biotechnol. 2001;3:113-22 pubmed
    ..Interestingly in all the cases examined the tolQ and tolR genes or their homologues appear to be present as a pair, with a potential for a tight translational regulation. ..
  8. Derouiche R, Benedetti H, Lazzaroni J, Lazdunski C, Lloubes R. Protein complex within Escherichia coli inner membrane. TolA N-terminal domain interacts with TolQ and TolR proteins. J Biol Chem. 1995;270:11078-84 pubmed
    The TolA, TolB, TolQ, and TolR proteins are involved in maintaining the integrity of the Escherichia coli outer membrane and in the import of group A colicins and filamentous phage DNA...
  9. Clavel T, Germon P, Vianney A, Portalier R, Lazzaroni J. TolB protein of Escherichia coli K-12 interacts with the outer membrane peptidoglycan-associated proteins Pal, Lpp and OmpA. Mol Microbiol. 1998;29:359-67 pubmed
    ..Transmembrane domains of TolQ, TolR and TolA interact in the cytoplasmic membrane, while TolB and Pal form a complex near the outer membrane...
  10. Walburger A, Lazdunski C, Corda Y. The Tol/Pal system function requires an interaction between the C-terminal domain of TolA and the N-terminal domain of TolB. Mol Microbiol. 2002;44:695-708 pubmed
    The Tol/Pal system of Escherichia coli is composed of the YbgC, TolQ, TolA, TolR, TolB, Pal and YbgF proteins...
  11. Germon P, Ray M, Vianney A, Lazzaroni J. Energy-dependent conformational change in the TolA protein of Escherichia coli involves its N-terminal domain, TolQ, and TolR. J Bacteriol. 2001;183:4110-4 pubmed
    TolQ, TolR, and TolA inner membrane proteins of Escherichia coli are involved in maintaining the stability of the outer membrane. They share homology with the ExbB, ExbD, and TonB proteins, respectively...
  12. Webster R. The tol gene products and the import of macromolecules into Escherichia coli. Mol Microbiol. 1991;5:1005-11 pubmed
    ..coli. Information is also available regarding the domains of the colicins or phage proteins which interact with the Tol proteins. A preliminary model of the location and possible interactions of the Tol proteins is presented. ..
  13. Vianney A, Muller M, Clavel T, Lazzaroni J, Portalier R, Webster R. Characterization of the tol-pal region of Escherichia coli K-12: translational control of tolR expression by TolQ and identification of a new open reading frame downstream of pal encoding a periplasmic protein. J Bacteriol. 1996;178:4031-8 pubmed
    The TolQ, TolR, TolA, TolB, and Pal proteins appear to function in maintaining the integrity of the outer membrane, as well as facilitating the uptake of the group A colicins and the DNA of the infecting filamentous bacteriophages...
  14. Levengood Freyermuth S, Click E, Webster R. Role of the carboxyl-terminal domain of TolA in protein import and integrity of the outer membrane. J Bacteriol. 1993;175:222-8 pubmed
    The TolA protein is involved in maintaining the integrity of the outer membrane of Escherichia coli, as mutations in tolA cause the bacteria to become hypersensitive to detergents and certain antibiotics and to leak periplasmic proteins ..
  15. Deprez C, Lloubes R, Gavioli M, Marion D, Guerlesquin F, Blanchard L. Solution structure of the E.coli TolA C-terminal domain reveals conformational changes upon binding to the phage g3p N-terminal domain. J Mol Biol. 2005;346:1047-57 pubmed
    ..The TolA protein plays a central role in these import mechanisms...
  16. Anderluh G, Hong Q, Boetzel R, MacDonald C, Moore G, Virden R, et al. Concerted folding and binding of a flexible colicin domain to its periplasmic receptor TolA. J Biol Chem. 2003;278:21860-8 pubmed
    ..In this article we have studied binding of the colicin N translocation domain to its periplasmic receptor TolA, by fluorescence resonance energy transfer (FRET) using fluorescent probes attached to engineered cysteine residues ..
  17. Bonsor D, Hecht O, Vankemmelbeke M, Sharma A, Krachler A, Housden N, et al. Allosteric beta-propeller signalling in TolB and its manipulation by translocating colicins. EMBO J. 2009;28:2846-57 pubmed publisher
    ..govern two conformational states that are adopted by the distal N-terminal 12 residues of TolB that bind TolA in the inner membrane. ColE9 promotes disorder of this 'TolA box' and recruitment of TolA...
  18. Gokce I, Raggett E, Hong Q, Virden R, Cooper A, Lakey J. The TolA-recognition site of colicin N. ITC, SPR and stopped-flow fluorescence define a crucial 27-residue segment. J Mol Biol. 2000;304:621-32 pubmed
    ..After first binding to the outer membrane surface receptors via their central region, they interact with TolA or TonB proteins via their N-terminal region...
  19. Fognini Lefebvre N, Lazzaroni J, Portalier R. tolA, tolB and excC, three cistrons involved in the control of pleiotropic release of periplasmic proteins by Escherichia coli K12. Mol Gen Genet. 1987;209:391-5 pubmed
    ..Furthermore, we identified a third cistron, excC, involved in the excretion of periplasmic enzymes but distinct from the two others.
  20. Gaspar J, Thomas J, Marolda C, Valvano M. Surface expression of O-specific lipopolysaccharide in Escherichia coli requires the function of the TolA protein. Mol Microbiol. 2000;38:262-75 pubmed
    ..The tolA and tolQ mutants showed reduced O7 LPS expression compared with the respective isogenic parent strains...
  21. Deprez C, Blanchard L, Guerlesquin F, Gavioli M, Simorre J, Lazdunski C, et al. Macromolecular import into Escherichia coli: the TolA C-terminal domain changes conformation when interacting with the colicin A toxin. Biochemistry. 2002;41:2589-98 pubmed
    ..However, this second step is poorly understood. It was shown that the TolA, TolQ, and TolR proteins play a critical role in the translocation of group A colicins and filamentous ..
  22. Hecht O, Ridley H, Boetzel R, Lewin A, Cull N, Chalton D, et al. Self-recognition by an intrinsically disordered protein. FEBS Lett. 2008;582:2673-7 pubmed publisher
    ..here that the specific 27 consecutive residues of the T-domain of colicin N known to bind to the helper protein TolA in target cells also interacts intramolecularly with folded regions of colicin N...
  23. Karlsson F, Malmborg Hager A, Borrebaeck C. Escherichia coli TolA tolerates multiple amino-acid substitutions as revealed by screening randomized variants for membrane integrity and phage receptor function. FEMS Microbiol Lett. 2006;259:81-8 pubmed
    Escherichia coli TolA is a cytoplasmic membrane protein required for outer membrane integrity and the translocation of F-specific filamentous (Ff) bacteriophage DNA...
  24. Karlsson F, Borrebaeck C, Nilsson N, Malmborg Hager A. The mechanism of bacterial infection by filamentous phages involves molecular interactions between TolA and phage protein 3 domains. J Bacteriol. 2003;185:2628-34 pubmed
    ..The molecular interactions between these domains and the known bacterial coreceptor protein (TolA) were studied using a biosensor technique, and we report here on interactions of the viral coat protein with TolA, ..
  25. Davies J, Reeves P. Genetics of resistance to colicins in Escherichia coli K-12: cross-resistance among colicins of group A. J Bacteriol. 1975;123:102-17 pubmed
    ..We have confirmed the position of previously isolated mutations on the Escherichia coli K-12 genetic map, and located approximately the loci conferring colicin resistance in some of the newly isolated mutants. ..
  26. Lubkowski J, Hennecke F, Pluckthun A, Wlodawer A. Filamentous phage infection: crystal structure of g3p in complex with its coreceptor, the C-terminal domain of TolA. Structure. 1999;7:711-22 pubmed
    ..3 protein (g3p) with the bacterial F pilus (primary receptor), and subsequently with the integral membrane protein TolA (coreceptor). G3p consists of three domains (N1, N2, and CT)...
  27. Li C, Zhang Y, Vankemmelbeke M, Hecht O, Aleanizy F, MacDonald C, et al. Structural evidence that colicin A protein binds to a novel binding site of TolA protein in Escherichia coli periplasm. J Biol Chem. 2012;287:19048-57 pubmed publisher
    ..b>TolA is central to this network linking the inner and outer membranes by interactions with TolQ, TolR, TolB, and Pal...
  28. Sharma O, Datsenko K, Ess S, Zhalnina M, Wanner B, Cramer W. Genome-wide screens: novel mechanisms in colicin import and cytotoxicity. Mol Microbiol. 2009;73:571-85 pubmed publisher
    ..Of the tol genes that function in the cytoplasmic membrane translocon, colE1 requires tolA and tolR but not tolQ for activity...
  29. Hecht O, Ridley H, Lakey J, Moore G. A common interaction for the entry of colicin N and filamentous phage into Escherichia coli. J Mol Biol. 2009;388:880-93 pubmed publisher
    Colicin N is a pore-forming bacteriocin that enters target Escherichia coli cells with the assistance of TolA, a protein in the periplasm of the target cell...
  30. Weitzel A, Larsen R. Differential complementation of DeltatolA Escherichia coli by a Yersinia enterocolitica TolA homologue. FEMS Microbiol Lett. 2008;282:81-8 pubmed publisher
    ..Central to this system is TolA, which spans the periplasmic space to communicate with residents of each membrane...
  31. Gerding M, Ogata Y, Pecora N, Niki H, de Boer P. The trans-envelope Tol-Pal complex is part of the cell division machinery and required for proper outer-membrane invagination during cell constriction in E. coli. Mol Microbiol. 2007;63:1008-25 pubmed
  32. Pommier S, Gavioli M, Cascales E, Lloubes R. Tol-dependent macromolecule import through the Escherichia coli cell envelope requires the presence of an exposed TolA binding motif. J Bacteriol. 2005;187:7526-34 pubmed
    ..This system forms protein complexes in which TolA plays a central role by providing a bridge between the inner and outer membranes via its interaction with the Pal ..
  33. Krachler A, Sharma A, Cauldwell A, Papadakos G, Kleanthous C. TolA modulates the oligomeric status of YbgF in the bacterial periplasm. J Mol Biol. 2010;403:270-85 pubmed publisher
    ..We have addressed this anomaly by characterizing YbgF from Escherichia coli and its interaction with TolA, which, based on previous yeast two-hybrid data, is the only known physical link between YbgF and the Tol system...
  34. Lazdunski C, Bouveret E, Rigal A, Journet L, Lloubes R, Benedetti H. Colicin import into Escherichia coli cells. J Bacteriol. 1998;180:4993-5002 pubmed
  35. Vianney A, Jubelin G, Renault S, Dorel C, Lejeune P, Lazzaroni J. Escherichia coli tol and rcs genes participate in the complex network affecting curli synthesis. Microbiology. 2005;151:2487-97 pubmed
    ..A recent survey of gene expression in Pseudomonas aeruginosa biofilms has identified tolA as a gene activated in biofilms...
  36. Ridley H, Lakey J. Antibacterial toxin colicin N and phage protein G3p compete with TolB for a binding site on TolA. Microbiology. 2015;161:503-15 pubmed publisher
    ..Group A colicins bind to members of the TolQRAB complex in the periplasm and heterotrimeric complexes of colicin-TolA-TolB have been observed for both ColA and ColE9...
  37. Cardelli J, Konisky J. Isolation and characterization of an Escherichia coli mutant tolerant to colicins Ia and Ib. J Bacteriol. 1974;119:379-85 pubmed
    ..The tolI mutant shows a reduced sensitivity to sodium azide and phenethylalcohol. It is suggested that tolI is deficient in some aspect of aerobic metabolism which must be operative for colicin I sensitivity. ..
  38. Bernard C, Sadasivam M, Shiomi D, Margolin W. An altered FtsA can compensate for the loss of essential cell division protein FtsN in Escherichia coli. Mol Microbiol. 2007;64:1289-305 pubmed
    ..b>TolA, which normally requires FtsN for its recruitment to the divisome, localized proficiently in the suppressed ftsN ..
  39. Sun T, Webster R. fii, a bacterial locus required for filamentous phage infection and its relation to colicin-tolerant tolA and tolB. J Bacteriol. 1986;165:107-15 pubmed
    ..The fii locus maps adjacent to tolA, mutants of which demonstrate tolerance to high levels of the E and K colicins...
  40. Davies J, Reeves P. Genetics of resistance to colicins in Escherichia coli K-12: cross-resistance among colicins of group B. J Bacteriol. 1975;123:96-101 pubmed
    ..Sodium dodecyl sulfate-polyacrylamide gel electrophoresis has revealed substantial changes in the composition of the outer membrane proteins of exbB and tonB mutants. ..
  41. Muller M, Webster R. Characterization of the tol-pal and cyd region of Escherichia coli K-12: transcript analysis and identification of two new proteins encoded by the cyd operon. J Bacteriol. 1997;179:2077-80 pubmed
    ..The cyd transcript contains cydA cydB followed by two open reading frames: orfC, encoding a 37-residue peptide, and orfD, encoding a 97-residue peptide. Both OrfC and OrfD are synthesized in minicells. ..
  42. Foulds J, Barrett C. Characterization of Escherichia coli mutants tolerant to bacteriocin JF246: two new classes of tolerant mutants. J Bacteriol. 1973;116:885-92 pubmed
    ..Two classes of mutants, class A and class B, are equivalent to tolA and tolB type mutants. We found tolA and tolB mutants were sensitive to the antibiotic bacitracin...
  43. Sun T, Webster R. Nucleotide sequence of a gene cluster involved in entry of E colicins and single-stranded DNA of infecting filamentous bacteriophages into Escherichia coli. J Bacteriol. 1987;169:2667-74 pubmed
    Mutations in fii or tolA of the fii-tolA-tolB gene cluster at 17 min on the Escherichia coli map render cells tolerant to high concentrations of the E colicins and do not allow the DNA of infecting single-stranded filamentous ..
  44. Rigal A, Bouveret E, Lloubes R, Lazdunski C, Benedetti H. The TolB protein interacts with the porins of Escherichia coli. J Bacteriol. 1997;179:7274-9 pubmed
    ..These interactions took place both in the presence and in the absence of lipopolysaccharide. TolA, an inner membrane component of the Tol system, also interacts with the trimeric porins via its central periplasmic ..
  45. Morgan J, Ortiz J, Riordan J. The role for TolA in enterohemorrhagic Escherichia coli pathogenesis and virulence gene transcription. Microb Pathog. 2014;77:42-52 pubmed publisher
    Loss of the periplasm spanning protein TolA in Escherichia coli leads to activation of the Rcs phosphorelay, and is required for full virulence in Gram-negative pathogens such as Salmonella enterica and Dickeya dadantii...
  46. Zhou K, Michiels C, Aertsen A. Variation of intragenic tandem repeat tract of tolA modulates Escherichia coli stress tolerance. PLoS ONE. 2012;7:e47766 pubmed publisher
    In recent work we discovered that the intragenic tandem repeat (TR) region of the tolA gene is highly variable among different Escherichia coli strains...
  47. Gully D, Bouveret E. A protein network for phospholipid synthesis uncovered by a variant of the tandem affinity purification method in Escherichia coli. Proteomics. 2006;6:282-93 pubmed
    ..Taken together, these results describe an integrated protein network that could be involved in the coordination of phospholipid metabolism. ..
  48. McBroom A, Johnson A, Vemulapalli S, Kuehn M. Outer membrane vesicle production by Escherichia coli is independent of membrane instability. J Bacteriol. 2006;188:5385-92 pubmed
    ..Detergent sensitivity, leakiness, and growth characteristics of the novel vesiculation mutant strains did not correlate with vesiculation levels, demonstrating that vesicle production is not predictive of envelope instability. ..
  49. Thomas J, Valvano M. Role of tol genes in cloacin DF13 susceptibility of Escherichia coli K-12 strains expressing the cloacin DF13-aerobactin receptor IutA. J Bacteriol. 1993;175:548-52 pubmed
    ..A. Valvano, FEMS Microbiol. Lett. 91:107-112, 1992). In this study, we demonstrate that the genes tolQ, tolR, and tolA, but not tolB, tolC, and ompF, are required for the internalization of cloacin DF13 and they are not involved in ..
  50. Vankemmelbeke M, Zhang Y, Moore G, Kleanthous C, Penfold C, James R. Energy-dependent immunity protein release during tol-dependent nuclease colicin translocation. J Biol Chem. 2009;284:18932-41 pubmed publisher
    ..components necessary for immunity protein release and found that in addition to a requirement for tolB, the tolA deletion strain was most affected...
  51. Barnéoud Arnoulet A, Gavioli M, Lloubes R, Cascales E. Interaction of the colicin K bactericidal toxin with components of its import machinery in the periplasm of Escherichia coli. J Bacteriol. 2010;192:5934-42 pubmed publisher
    ..of in vivo coimmunoprecipitations and in vitro pulldown experiments, we demonstrated that KT interacts with the TolA, TolB, and TolR proteins...
  52. Anderluh G, Gokce I, Lakey J. Expression of proteins using the third domain of the Escherichia coli periplasmic-protein TolA as a fusion partner. Protein Expr Purif. 2003;28:173-81 pubmed
    The third domain of the periplasmic protein TolA from Escherichia coli (TolAIII) was used as a fusion partner in the expression of various proteins from bacteria and eukaryotes...
  53. Derouiche R, Gavioli M, Benedetti H, Prilipov A, Lazdunski C, Lloubes R. TolA central domain interacts with Escherichia coli porins. EMBO J. 1996;15:6408-15 pubmed
    b>TolA is an inner membrane protein with three domains: a transmembrane N-terminus and periplasmic central and C-terminal domains. The interaction of TolA with outer membrane porins of Escherichia coli was investigated...
  54. Henry T, Pommier S, Journet L, Bernadac A, Gorvel J, Lloubes R. Improved methods for producing outer membrane vesicles in Gram-negative bacteria. Res Microbiol. 2004;155:437-46 pubmed
    ..of Escherichia coli, required to maintain outer membrane integrity, is composed of five cell envelope proteins, TolA, TolB, TolQ, TolR and Pal. Tol proteins are parasitized by filamentous bacteriophages and by colicins...
  55. Braun V, Frenz J, Hantke K, Schaller K. Penetration of colicin M into cells of Escherichia coli. J Bacteriol. 1980;142:162-8 pubmed
    ..These data suggest that the function controlled by the tonB gene is required for the translocation of colicin M from its initial binding site at the tonA-coded receptor protein to the target. ..