The efficient export of NADP-containing glucose-fructose oxidoreductase to the periplasm of Zymomonas mobilis depends both on an intact twin- arginine motif in the signal peptide and on the generation of a structural export signal induced by cofactor binding

European Journal of Biochemistry

Volumn 263, Issue 2, 1999, Pages 543-551

  Halbig, Dirk ^a   Wiegert, Thomas ^b   Blaudeck, Natascha ^a   Freudl, Roland ^a   Sprenger, Georg A ^a  

^a FORSCHUNGSZENTRUM JÜLICH   (Germany)

^b UNIVERSITY OF BAYREUTH   (Germany)

Author keywords

Cofactor binding; Protein export; Sec independent translocation; Signal peptide; Twin arginine motif

Indexed keywords

ARGININE; BETA GALACTOSIDASE; FRUCTOSE; GLUCOSE; HYBRID PROTEIN; MUTANT PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; OXIDOREDUCTASE; SIGNAL PEPTIDE;

AMINO ACID SUBSTITUTION; ARTICLE; CONFORMATIONAL TRANSITION; CYTOPLASM; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN STRUCTURE; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; ZYMOMONAS MOBILIS;

ARGININE; ESCHERICHIA COLI; MODELS, BIOLOGICAL; MUTAGENESIS, SITE-DIRECTED; NADP; OXIDATION-REDUCTION; OXIDOREDUCTASES; PERIPLASM; PROTEIN BINDING; PROTEIN FOLDING; RECOMBINANT FUSION PROTEINS; TIME FACTORS; ZYMOMONAS;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; ZYMOMONAS MOBILIS;

EID: 0033565687     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1327.1999.00536.x     Document Type: Article

References (56)

1. 1. Pugsley, A.P. (1993) The complete general secretory pathway in Gram-negative bacteria. Microbiol. Rev. 57, 50-108.
2. 2. Driessen, A.J.M. (1994) How proteins cross the bacterial cytoplasmic membrane. J. Membr. Biol. 142, 145-159.
3. 3. Wickner, W. & Rice-Leonard, M. (1996) Escherichia coli preprotein translocase. J. Biol. Chem. 271, 29514-29516.
4. 4. Von Heijne, G. (1990) The signal peptide. J. Membr. Biol. 115, 195-201.
5. 5. Pohlschröder, M., Prinz, W.A., Hartmann, E. & Beckwith, J. (1997) Protein translocation in the three domains of life: variations on a theme. Cell 91, 563-566.
6. 6. Randall, L.L. & Hardy, S.L.S. (1986) Correlation of competence for export with lack of tertiary structure of the mature species: a study in vivo of maltose-binding protein in E. coli. Cell 46, 921-928.
7. 7. Kumamoto, C.A. (1991) Molecular chaperones and protein translocation across the Escherichia coli inner membrane. Mol. Microbiol. 5, 19-22.
8. 8. Freudl, R., Schwarz, H., Kramps, S., Hindennach, I. & Henning, U. (1988) Dihydrofolate reductase (mouse) and β-galactosidase (Escherichia coli) can be translocated across the plasma membrane of E. coli. J. Biol. Chem. 263, 17084-17091.
9. 9. Arkowitz, R.A., Joly, J.C. & Wickner, W. (1993) Translocation can drive the unfolding of a preprotein domain. EMBO J. 12, 243-253.
10. 10. Berks, B.C. (1996) A common export pathway for proteins binding complex redox cofactors? Mol. Microbiol. 22, 393-404.
11. 11. Santini, C.-L., Ize, B., Chanal, A., Müller, M., Giordano, G. & Wu, L.-F. (1998) A novel Sec-independent periplasmic protein translocation pathway in Escherichia coli. EMBO J. 17, 101-112.
12. 12. Weiner, J.H., Bilous, P.T., Shaw, G.M., Lubitz, S.P., Frost, L., Thomas, G.H., Cole, J.A. & Turner, R.J. (1998) A novel and ubiquitous system for membrane targeting and secretion of cofactor-containing proteins. Cell 93, 93-101.
13. 13. Bogsch, E.G., Sargent, F., Stanley, N.R., Berks, B.C., Robinson, C. & Palmer, T. (1998) An essential component of a novel bacterial protein export system with homologues in plastids and mitochondria. J. Biol. Chem. 273, 18003-18006.
14. 14. Sargent, F., Bogsch, E.G., Stanley, N.R., Wexler, M., Robinson, C., Berks, B.C. & Palmer, T. (1998) Overlapping functions of components of a bacterial Sec-independent protein export pathway. EMBO J. 17, 3640-3650.
15. 15. Nivière, V., Wong, S.L. & Voordouw, G. (1992) Site-directed mutagenesis of the hydrogenase signal peptide consensus box prevents export of a β-lactamase fusion protein. J. Gen. Microbiol. 138, 2173-2183.
16. 16. Dreusch, A., Burgisser, D.M., Heizmann, C.W. & Zumft, W.G. (1997) Lack of copper insertion into unprocessed cytoplasmic nitrous oxide reductase generated by an R20D substitution in the arginine consensus motif of the signal peptide. Biochim. Biophys. Acta 1319, 311-318.
17. 17. Chaddock, A.M., Mant, A., Karnauchov, I., Brink, S., Herrmann, R.G., Klösgen, R.B. & Robinson, C. (1995) A new type of signal peptide: central role of a twin-arginine motif in transfer signals for the delta pH-dependent thylakoidal protein translocase. EMBO J. 14, 2715-2722.
18. 18. Robinson, C. & Mant, A. (1997) Targeting of proteins into and across the thylakoid membrane. Trends Plant Sci. 2, 431-437.
19. 19. Rodrigue, A., Boxer, D.H., Mandrand-Berthelot, M.A. & Wu, L.F. (1996) Requirement for nickel of the transmembrane translocation of NiFe-hydrogenase 2 in Escherichia coli. FEBS Lett. 392, 81-86.
20. 20. Loos, H., Völler, M., Rehr, B., Stierhof, Y.-D., Sahm, H. & Sprenger, G.A. (1991) Localisation of the glucose-fructose oxidoreductase in wild type and overproducing strains of Zymomonas mobilis. FEMS Microbiol. Lett. 84, 211-216.
21. 21. Kanagasundaram, V. & Scopes, R.K. (1992) Cloning, sequence analysis, and expression of the structural gene encoding glucose-fructose oxidoreductase from Zymomonas mobilis. J. Bacteriol. 174, 1439-1447.
22. 22. Wiegert, T., Sahm, H. & Sprenger, G.A. (1996) Export of the periplasmic NADP-containing glucose-fructose oxidoreductase of Zymomonas mobilis. Arch. Microbiol. 166, 32-41.
23. 23. Zachariou, M. & Scopes, R.K. (1986) Glucose-fructose oxidoreductase, a new enzyme isolated from Zymomonas mobilis that is responsible for sorbitol production. J. Bacteriol. 167, 863-869.
24. 24. Kingston, R.L., Scopes, R.K. & Baker, E.N. (1996) The structure of glucose-fructose oxidoreductase from Zymomonas mobilis: an osmoprotective periplasmic enzyme containing nondissociable NADP. Structure 4, 1413-1428.
25. 25. Loos, H., Sahm, H. & Sprenger, G.A. (1993) Glucose-fructose oxidoreductase, a periplasmic enzyme of Zymomonas mobilis, is active in its precursor form. FEMS Microbiol. Lett. 107, 293-298.
26. 26. Yanisch-Perron, C., Vieira, J. & Messing, J. (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33, 103-119.
27. 27. Simon, R., Priefer, U. & Pühler, A. (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram-negative bacteria. Biotechnology 1, 784-790.
28. 28. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
29. 29. de Goncalves Lima, O., Schumacher, I.E. & de Aranjo, J.M. (1972) New observations about the antagonistic effects of Zymomonas mobilis var. recifensis. Rev. Inst. Antibiot. Uni. Recife 12, 57-69.
30. 30. Bolivar, F., Rodriguez, R.L., Greene, P.J., Betlach, M.C., Heynecker, H.L., Boyer, H.W., Crosa, J.H. & Falkow, S. (1977) Construction and characterization of new cloning vehicles II. A multipurpose cloning system. Gene 2, 95-113.
31. 31. Shapira, S.K., Cou, J., Richaud, F.V. & Casadaban, M.J. (1983) New versatile plasmid vectors for expression of hybrid proteins coded by a cloned gene fused to lacZ-gene sequences encoding an enzymatically active carboxy-termined portion of beta-galactosidase. Gene 25, 71-82.
32. 32. Hanahan, D. (1983) Studies on the transformation of Escherichia coli with plasmids. J. Mol. Biol. 166, 557-580.
33. 33. Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989) Molecular Cloning. A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
34. 34. Sanger, F., Nicklen, S. & Coulson, A.R. (1977) DNA sequencing with chain termination inhibitors. Proc. Natl Acad. Sci. USA 74, 5463-5467.
35. 35. Kunkel, T.A. (1985) Rapid and efficient site specific mutagenesis without phenotypic selection. Proc. Natl Acad. Sci. USA 82, 488-492.
36. 36. Wiegert, T., Sahm, H. & Sprenger, G.A. (1997) The substitution of a single amino acid residue (Ser116Asp) alters NADP-containing glucose-fructose oxidoreductase of Zymomonas mobilis into a glucose dehydrogenase with dual coenzyme specificity. J. Biol. Chem. 272, 13126-13133.
37. 37. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principles of protein dye-binding. Anal. Biochem. 72, 248-254.
38. 38. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
39. 39. Towbin, H.T., Staehelin, T. & Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl Acad. Sci. USA 76, 4350-4354.
40. 40. Ito, K., Bassford, P.J. & Beckwith, J. (1981) Protein localization in E. coli: is there a common step in the secretion of periplasmic and outer-membrane proteins? Cell 24, 707-717.
41. 41. Gebert, J.F., Overhoff, B., Manson, M.D. & Boos, W. (1988) The chemosensory transducer of Escherichia coli assembles into the cytoplasmic membrane via a SecA-dependent process. J. Biol. Chem. 263, 16652-16660.
42. 42. Neu, H.C. & Heppel, L.A. (1965) The release of enzymes from Escherichia coli by osmotic shock and during the formation of spheroplasts. J. Biol. Chem. 240, 3685-3692.
43. 43. Wiegert, T., Sahm, H. & Sprenger, G.A. (1997) Expression of the Zymomonas mobilis gfo gene for NADP-containing glucose: fructose oxidoreductase (GFOR) in Escherichia coli. Formation of enzymatically active preGFOR but lack of processing into a stable periplasmic protein. Eur. J. Biochem. 244, 107-112.
44. 44. Loos, H., Ermler, U., Sprenger, G.A. & Sahm, H. (1994) Crystallization and preliminary X-ray analysis of glucose-fructose oxidoreductase from Zymomonas mobilis. Protein Sci. 3, 2447-2449.
45. 45. Tjalsma, H., Kontinen, V.P., Prágai, Z., Wu, H., Meima, R., Venema, G., Bron, S., Sarvas, M. & van Dijl, J.M. (1999) The role of lipoprotein processing by signal peptidase II in the Gram-positive eubacterium Bacillus subtilis. J. Biol. Chem. 274, 1698-1707.
46. 46. Bassford Jr, P.J., Silhavy, T.J. & Beckwith, J.R. (1979) Use of gene fusions to study secretion of maltose-binding protein into Escherichia coli periplasm. J. Bacteriol. 139, 19-31.
47. 47. Rasmussen, B.A. & Bankaitis, V.A. & Bassford Jr, P.J. (1984) Export and processing of MaIE-LacZ hybrid proteins in Escherichia coli. J. Bacteriol. 160, 612-617.
48. 48. Tommassen, J., Leunissen, J., Van Damme-Jongsten, M. & Overduin, P. (1985) Failure of E. coli K-12 to transport phoE-lacZ fusion proteins out of the cytoplasm. EMBO J. 4, 1041-1047.
49. 49. Ito, K., Akiyama, Y., Yura, T. & Shiba, K. (1986) Diverse effects of the MaIE-LacZ hybrid protein on Escherichia coli cell physiology. J. Bacteriol. 167, 201-220.
50. 50. Voorhout, W., de Kroon, T., Leunissen-Bijvelt, J., Verkleij, A. & Tommassen, J. (1988) Accumulation of LamB-LacZ hybrid proteins in intracytoplasmic membrane-like structures in Escherichia coli K-12. J. Gen. Microbiol. 134, 599-604.
51. 51. Kiino, D.R., Phillips, G.J. & Silhavy, T.J. (1990) Increased expression of the bifunctional protein PrIF suppresses overproduction lethality associated with exported β-galactosidase hybrid proteins in Escherichia coli. J. Bacteriol. 172, 185-192.
52. 52. Snyder, W.B. & Silhavy, T.J. (1995) β-galactosidase is inactivated by intermolecular disulfide bonds and is toxic when secreted to the periplasm of Escherichia coli. J. Bacteriol. 177, 953-963.
53. 53. Henry, R., Carrigan, M., McCaffery, M., Ma, X. & Cline, K. (1997) Targeting determinants and proposed evolutionary basis for the Sec and the delta pH protein transport systems in chloroplast thylakoid membranes. J. Cell. Biol. 136, 823-832.
54. 54. Fortin, Y., Phoenix, P. & Drapeau, G.R. (1990) Mutations conferring resistance to azide in Escherichia coli occur primarily in the secA gene. J. Bacteriol. 172, 6607-6610.
55. 55. Oliver, D.B., Cabelli, R.J., Dolan, K.M. & Jarosik, G.P. (1990) Azide-resistant mutants of Escherichia coli alter the SecA protein, an azide-sensitive component of the protein export machinery. Proc. Natl Acad. Sci. USA 87, 8227-8231.
56. 56. Klein, M., Hofmann, B., Klose, M. & Freudl, R. (1994) Isolation and characterization of a Bacillus subtilis secA mutant allele conferring resistance to sodium azide. FEMS Microbiol. Lett. 124, 393-398.