A novel DnaJ-like protein in Escherichia coli inserts into the cytoplasmic membrane with a Type III topology

Molecular Microbiology

Volumn 20, Issue 6, 1996, Pages 1273-1286

  Clarke, David J ^a   Jacq, A ^a   Holland, I B ^a  

^a CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CHAPERONE; KANAMYCIN; MEMBRANE PROTEIN; PROTEIN ANTIBODY; SPECTINOMYCIN; TRYPSIN;

AMINO ACID SEQUENCE; ANTIBODY PRODUCTION; ARTICLE; BACTERIAL GENETICS; BACTERIAL GROWTH; COXIELLA BURNETII; DIMERIZATION; DNA REPLICATION; ESCHERICHIA COLI; HAEMOPHILUS INFLUENZAE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN LOCALIZATION; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, BACTERIAL; BACTERIAL PROTEINS; CELL EXTRACTS; CELL MEMBRANE; CULTURE MEDIA; CYTOSKELETAL PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HEAT-SHOCK PROTEINS; HSP40 HEAT-SHOCK PROTEINS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; POLYSACCHARIDES; POLYSACCHARIDES, BACTERIAL; RABBITS; RECOMBINANT FUSION PROTEINS;

BACTERIA (MICROORGANISMS); COXIELLA BURNETII; COXIELLA BURNETTI; ESCHERICHIA COLI; EUKARYOTA; HAEMOPHILUS INFLUENZAE;

EID: 0029900569     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.1996.tb02646.x     Document Type: Article

References (64)

1. Andersson, H., and von Heijne, H.G. (1993) Sec dependent and sec independent assembly of E. coli inner membrane proteins: the topological rules depend on chain length. FMBO J 12: 683-691.
2. + on the translocation of charged residues explain the 'positive inside' rule. EMBO J 13: 2267-2272.
3. van Asseldonk, M., Simons, A., Visser, H., de Vos, W., and Simons, G. (1993) Cloning, nucleotide sequence, and regulatory analysis of the Lactococcus lactis dnaJ gene. J Bacteriol 175: 1637-1644.
4. Behrens, S., Narbemaus, F., and Bahl, H. (1993) Cloning, nucleotide sequence and structural analysis of the Clostridium acetobutylicum dnaJ gene. FEMS Microbiol Lett 114: 53-60.
5. Bessoule, J.J. (1993) Occurrence and sequence of a DnaJ protein in plant (Allium porrum) epidermal cells. FEBS Lett 323: 51-54.
6. Blumberg, H., and Silver, P.A. (1991) A homologue of the bacterial heat-shock gene DnaJ that alters protein sorting in yeast. Nature 349: 627-630.
7. Bork, P., Sander, C., Valencia, A., and Bukau, B. (1992) A module of the DnaJ heat shock proteins found in malaria parasites. Trends Biochem Sci 17: 129.
8. Brodsky, J.L., and Schekman, R. (1993) A Sec63p-BiP complex from yeast is required for protein translocation in a reconstituted proteoliposome. J Cell Biol 123: 1355-1363.
9. Bukau, B. (1993) Regulation of the Escherichia coli heat-shock response. Mol Microbiol 9: 671-680.
10. Cao, G., and Dalbey, R.E. (1994) Translocation of N-terminal tails across the plasma membrane. EMBO J 13: 4662-4669.
11. Cao, G., Kuhn, A., and Dalbey, R.E. (1995) The translocation of negatively charged residues across the membrane is driven by the electrochemical potential: evidence for an electrophoresis-like membrane transfer mechanism. EMBO J 14: 866-875.
12. Casaregola, S., Chen, M., Bouquin, N., Norris, V., Jacq, A., Goldberg, M., Margarson, S., Tempete, M., McKenna, S., Sweetman, H., Bernard, S., McGurk, G., Seror, S., and Holland, I.B. (1991) Analysis of a myosin-like protein and the role of calcium in the E. coli cell cycle. Res Microbiol 142: 201-207.
13. Chellaiah, A., Davis, A., and Mohanakumar, T. (1993) Cloning of a unique human homologue of the Escherichia coli DnaJ heat shock protein. Biochim Biophys Acta 1174: 111-113.
14. Chen, R., Schmidmayr, W., Krämer, C., Chen-Schmeisser, U., and Henning, U. (1980) Primary structure of major outer membrane protein II* (OmpA protein) of Escherichia coli K-12. Proc Natl Acad Sci USA 77: 4592-4596.
15. Danese, P.N., Snyder, W.B., Cosma, C.L., Davis, L.J., and Silhavy, T.J. (1995) The Cpx two-component signal transduction pathway of Escherichia coli regulates transcription of the gene specifying the stress-inducible periplasmic protease, DegP. Genes Dev 9: 387-398.
16. Darby, N.J., and Creighton, T.E. (1993) Protein Structure. In Focus. Rickwood, D. (ed.). Oxford: IRL Press.
17. Feldheim, D., Rothblatt, J., and Schekman, R. (1992) Topology and functional domains of Sec63p, an endoplasmic reticulum membrane protein required for secretory protein translocation. Mol Cell Biol 12: 3288-3296.
18. Filip, C., Fletcher, G., Wulff, J.L., and Earhart, C.F. (1973) Solubilisation of the inner membrane of E. coli by the ionic detergent sodium lauryl sarcosinate. J Bacteriol 115: 717-722.
19. Fleischmann, R.D. et al. (1995) Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269: 496-512.
20. Gayda, R.C., Henk, M.C., and Leong, D. (1992) C-shaped cells caused by expression of an ftsA mutation in Escherichia coli. J Bacteriol 174: 5362-5370.
21. Georgopoulos, C.P., Lundquist, H.A., Yochem, J., and Feiss, M. (1980) Identification of the E. coli dnaJ gene product. Mol Gen Genet 178: 583-588.
22. Gervais, F.G., and Drapeau, G.R. (1992) Identification, cloning, and characterization of rcsF, a new regulator gene for exopolysaccharide synthesis that suppresses the division mutation ftsZ84 in Escherichia coli K-12. J Bacteriol 174: 8016-8022.
23. Gervais, F.G., Phoneix, P., and Drapeau, G.R. (1992) The rcsB gene, a positive regulator of colanic acid biosynthesis in Escherichia coli, is also an activator of ftsZ expression. J Bacteriol 174: 3964-3971.
24. Gottesman, S., and Stout, V. (1991) Regulation of capsular polysaccharide synthesis in Escherichia coli K-12. Mol Microbiol 5: 1599-1606.
25. Halegoua, S., and Inouye, M. (1979) Translocation and assembly of outer membrane proteins of E. coli. J Mol Biol 130: 39-61.
26. Hendrick, J.P., Langer, T., Davis, T.A., Hartl, F.U., and Wiedmann, M. (1993) Control of folding and membrane translocation by binding of the chaperone DnaJ to nascent polypeptides. Proc Natl Acad Sci USA 90: 10216-10220.
27. von Heijne, G. (1992) Membrane protein structure prediction. Hydrophobicity analysis and the positive-inside rule. J Mol Biol 225: 487-494.
28. Hiraga, S., Niki, H., Ogura, T., Ichinose, C., Mori, H., Ezaki, B., and Jaffe, A. (1989) Chromosome partitionning in Escherichia coli: novels mutants producing anucleate cells. J Bacteriol 171: 1496-1505.
29. Hohfeld, J., and Hartl, F.U. (1994) Post-translational protein import and folding. Curr Opin Cell Biol 6: 499-509.
30. Ishidate, K., Creeger, E.S., Zrike, J., Deb, S., Glauner, B., MacAlister, T.J., and Rothfield, L.I. (1986) Isolation of differentiated membrane domains from Escherichia coli and Salmonella typhimurium, including a fraction containing attachment sites between the inner and outer membranes and the murein skeleton of the cell envelope. J Biol Chem 261: 428-443.
31. Kelley, W.L., and Landry, S.J. (1994) Chaperone power in a virus? Trends Biochem Sci 19: 277-278.
32. Kudlicki, W., Odom, O.W., Kramer, G., and Hardesty, B. (1994) Chaperone-dependent folding and activation of ribosome-bound nascent rhodanese. Analysis by fluorescence. J Mol Biol 2444: 319-331.
33. Laemmli, M.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
34. Lemmon, M.A., and Engelman, D.M. (1994) Specificity and promiscuity in membrane helix interactions. FEBS Lett 346: 17-20.
35. Lemmon, M.A., Treutlein, H.R., Adams, P.D., Brunger, A.T., and Engelman, D.M. (1994) A dimerization motif for transmembrane alpha-helices. Nat Struct Biol 1: 157-163.
36. Liberek, K., Marszalek, J., Ang, D., Georgopoulos, C., and Zylicz, M. (1991) Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc Natl Acad Sci USA 88: 2874-2878.
37. Ma, D., Cook, D.N., Alberti, M., Pon, N.G., Nikaido, H., and Hearst, J.E. (1993) Genes acrA and acrB encode a stress-induced efflux system of Escherichia coli. Mol Microbiol 16: 45-55.
38. E, an Escherichia coli heat-inducible sigma factor, is modulated by expression of outer membrane proteins. Genes Dev 7: 2618-2628.
39. Michel, H., Weyer, K.A., Gruenberg, H., and Lottspeich, F. (1985) The 'heavy' subunit of the photosynthetic reaction centre from Rhodopseudomonas viridis: isolation of the gene, nucleotide and amino acid sequence. EMBO J 4: 1667-1672.
40. Miller, J.H. (1992) A Short Course in Bacterial Genetics: A Laboratory Manual and Handbook for Escherichia coli and Related Bacteria. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
41. Nilsson, I., and von Heijne, H.G. (1990) Fine-tuning the topology of a polytopic membrane protein: role of positively and negatively charged amino acids. Cell 62: 1135-1141.
42. Osborn, M.J., Gander, J.E., Parisi, E., and Carson, J. (1972) Mechanism of assembly of the outer membrane of Salmonella typhimurium. Isolation and characterization of cytoplasmic and outer membrane. J Biol Chem 247: 3962-3972.
43. Pla, J., Sanchez, M., Palacios, P., Vicente, M., and Aldea, M. (1991) Preferential cytoplasmic location of FtsZ, a protein essential for Escherichia coli septation. Mol Microbiol 5: 1681-1686.
44. Prentki, P., and Krisch, H.M. (1984) In vitro insertional mutagenesis with a selectable DNA fragment. Gene 29: 303-313.
45. Rohrer, J., and Kuhn, A. (1990) The function of a leader peptide in translocating charged amino acyl residues across a membrane. Science 250: 1418-1421.
46. Rost, B., and Sander, C. (1993) Prediction of protein structure at better than 70% accuracy. J Mol Biol 232: 584-589.
47. Rost, B., and Sander, C. (1994) Combining evolutionary information and nueral networks to predict protein secondary structure. Proteins 19: 55-72.
48. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
49. Schlenstedt, G., Harris, S., Risse, B., Lill, R., and Silver, P.A. (1995) A yeast DnaJ homologue, Scj1p, can function in the endoplasmic reticulum with BiP/Kar2p via a conserved domain that specifies interactions with Hsp70s. J Cell Biol 129: 979-988.
50. Scidmore, M.A., Okamura, H.H., and Rose, M.D. (1993) Genetic interactions between KAR2 and SEC63, encoding eukaryotic homologues of DnaK and DnaJ in the endoplasmic reticulum. Mol Biol Cell 4: 1145-1159.
51. Sell, S.M., Eisen, C., Ang, D., Zylicz, M., and Georgopoulos, C. (1990) Isolation and characterization of dnaJ null mutants of Escherichia coli. J Bacteriol 172: 4827-4835.
52. Silver, P.A., and Way, J.C. (1993) Eukaryotic DnaJ homologs and the specificity of Hsp70 activity. Cell 74: 5-6.
53. Sternberg, M.J., and Gullick, W.J. (1990) A sequence motif in the transmembrane region of growth factor receptors with tyrosine kinase activity mediates dimerization. Protein Eng 3: 245-248.
54. Stoker, N.G., Fairweather, N.F., and Spratt, B.G. (1982) Versatile low-copy number plasmid vectors for cloning in Escherichia coli. Gene 18: 335-341.
55. Szabo, A., Langer, T., Schroder, H., Flanagan, J., Bukau, B., and Hartl, F.U. (1994) The ATP hydrolysis-dependent reaction cycle of the Escherichia coli Hsp70 system DnaK, DnaJ, and GrpE. Proc Natl Acad Sci USA 91: 10345-10349.
56. Ueguchi, C., Kakeda, M., Yamada, H., and Mizuno, T. (1994) An analogue of the DnaJ molecular chaperone in Escherichia coli. Proc Natl Acad Sci USA 91: 1054-1058.
57. Ueguchi, C., Shiozawa, T., Kakeda, M., Yamada, H., and Mizuno, T. (1995) A study of the double mutation of dnaJ and cbpA, whose gene products function as molecular chaperones in Escherichia coli. J Bacteriol 177: 3894-3896.
58. 2-terminal 108 amino acids of the Escherichia coli DnaJ protein stimulate the activity of DnaK and are sufficient for λ replication. J Biol Chem 269: 5446-5451.
59. Wetzstein, M., Volker, U., Dedio, J., Lobau, S., Zuber, U., Schiesswohl, M., Herget, C., Hecker, M., and Schumann, W. (1992) Cloning, sequencing, and molecular analysis of the dnaK locus from Bacillus subtilis. J Bacteriol 174: 3300-3310.
60. Whitley, P., Zander, T., Ehrmann, M., Haardt, M., Bremer, E., and von Heijne, H.G. (1994) Sec-independent translocation of a 100-residue periplasmic N-terminal tail in the E. coli inner membrane protein ProW. EMBO J 13: 4653-4661.
61. Wild, J., Altman, E., Yura, T., and Gross, C.A. (1992) DnaK and DnaJ heat shock proteins participate in protein export in Escherichia coli. Genes Dev 6: 1165-1172.
62. Yura, T., Mori, H., Nagai, H., Nagata, T., Ishihama, A., Fujita, N., Isono, K., Mizobuchi, K., and Nakata, A. (1992) Systematic sequencing of the Escherichia coli genome: analysis of the 0-2.4 min region. Nucl Acids Res 20: 3305-3308.
63. Zhong, T., and Arndt, K.T. (1993) The yeast SIS1 protein, a DnaJ homolog, is required for the initiation of translation. Cell 73: 1175-1186.
64. Zuber, M., Hoover, T.A., and Court, D.L. (1995) Analysis of a Coxiella burnetti gene product that activates capsule synthesis in Escherichia coli: requirement for the heat shock chaperone DnaK and the two-component regulator RcsC. J Bacteriol 177: 4238-4244.