1887

Chapter 13 : The Toxin-Coregulated Pilus: Biogenesis and Function

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in
Zoomout

The Toxin-Coregulated Pilus: Biogenesis and Function, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555818364/9781555810672_Chap13-1.gif /docserver/preview/fulltext/10.1128/9781555818364/9781555810672_Chap13-2.gif

Abstract:

The best characterized pilus of is the toxin-coregulated pilus (TCP) described by Taylor and coworkers. The pilus is designated TCP, for toxin-coregulated pilus, and the pilin subunit is designated TcpA. Fusions to genes show reduced levels of pilin and lack pili on the cell surface. Therefore, these genes probably encode assembly and transport proteins required for pilus biogenesis. Further analyses of TcpE, TcpF, and TcpC function are discussed. Amino acid sequencing of gel-purified TcpA reveals an amino-terminal region that bears striking homology to type IV pilins, formerly referred to as N-methylphenylalanine pilins because of the modification present on their amino-terminal residues. Secretion of bacterial cell surface proteins composing macromolecular complexes occurs by a mechanism only recently elucidated in comparison to the initial stages of general prokaryotic protein export. The pathway for TCP biogenesis provides a model system for investigating these novel secretion processes. A number of the fusions initially isolated on the basis of loss of TCP expression still express the TcpA pilin but fail to assemble or secrete pili. Thus, these genes are postulated to encode proteins with biogenesis functions. The proteins PilF, PilT, and PilD, presumed to play a role in pilus biogenesis, share substantial homology to pilus assembly proteins of the same name from . Recent data suggest that the TcpC protein may contain novel functions independent of its hypothesized role in pilus biogenesis.

Citation: Kaufman M, Taylor R. 1994. The Toxin-Coregulated Pilus: Biogenesis and Function, p 187-202. In Wachsmuth I, Blake P, Olsvik Ø (ed), and Cholera. ASM Press, Washington, DC. doi: 10.1128/9781555818364.ch13

Key Concept Ranking

Type IV Pili
0.488432
Outer Membrane Proteins
0.46077225
Integral Membrane Proteins
0.42369163
Transmission Electron Microscopy
0.41602454
0.488432
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of Figure 1
Figure 1

Electron micrograph of the TCP expressed by cultured at 30°C in Luria broth (pH 6.5) and negatively stained. Note the bundling of the pilus into large, hydrophobic masses.

Citation: Kaufman M, Taylor R. 1994. The Toxin-Coregulated Pilus: Biogenesis and Function, p 187-202. In Wachsmuth I, Blake P, Olsvik Ø (ed), and Cholera. ASM Press, Washington, DC. doi: 10.1128/9781555818364.ch13
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Organization of the TCP gene cluster. ?n insertions and relevant restriction sites are indicated at their approximate locations. Dark bars at the 5' ends of genes indicate the presence of a signal sequence as determined by PhoA fusion protein activity and nucleotide sequencing. Functions as determined by phenotypic analysis of mutants are listed under the genes. ORFs revealed by nucleotide sequencing are indicated by capital letters ( ). Arrows denote directions of transcription.

Citation: Kaufman M, Taylor R. 1994. The Toxin-Coregulated Pilus: Biogenesis and Function, p 187-202. In Wachsmuth I, Blake P, Olsvik Ø (ed), and Cholera. ASM Press, Washington, DC. doi: 10.1128/9781555818364.ch13
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3
Figure 3

Comparison of TcpA and other type IV pilins. Symbols: ■, residues in the majority of type PV pilins that are identical to TcpA; ○, conserved hydrophobic residues; arrow, pilin processing site. The hydrophobicity plot is a Kyte and Doolittle ( ) analysis for TcpA. The pattern is similar for all the pilins shown.

Citation: Kaufman M, Taylor R. 1994. The Toxin-Coregulated Pilus: Biogenesis and Function, p 187-202. In Wachsmuth I, Blake P, Olsvik Ø (ed), and Cholera. ASM Press, Washington, DC. doi: 10.1128/9781555818364.ch13
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 4
Figure 4

Active-site homologies between TcpG, PDI, thioredoxin, DsbA, and Por. TcpG residues 36 to 58 are aligned with the region surrounding the catalytic site (gray boxes) of rat liver PDI ( ), thioredoxin from ( ), the highly related DsbA protein of ( ), and the highly related Por protein of ( ).

Citation: Kaufman M, Taylor R. 1994. The Toxin-Coregulated Pilus: Biogenesis and Function, p 187-202. In Wachsmuth I, Blake P, Olsvik Ø (ed), and Cholera. ASM Press, Washington, DC. doi: 10.1128/9781555818364.ch13
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 5
Figure 5

Comparison of TcpJ function with leader peptidase. (A) During general export in , the N-terminal hydrophobic signal sequence of proteins to be translocated has a transmembrane orientation and is cleaved by signal peptidase I in the periplasm. (B) For secretion of TcpA, the hydrophilic leader peptide is likely to interact with the inner membrane and be cleaved on the cytoplasmic face. The membrane-embedded signal sequence for export is located in the mature pilin molecule. Cleavage of the basic leader could then allow release of pilin from the membrane for surface assembly, which is likely mediated by the products of additional TCP biogenesis genes. This figure has been reprinted with permission ( ).

Citation: Kaufman M, Taylor R. 1994. The Toxin-Coregulated Pilus: Biogenesis and Function, p 187-202. In Wachsmuth I, Blake P, Olsvik Ø (ed), and Cholera. ASM Press, Washington, DC. doi: 10.1128/9781555818364.ch13
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555818364.chap13
1. Albano, M.,, R. Briettling,, and D. A. Dubnau. 1989. Nucleotide sequence and genetic organization of the Bacillus subtilis comG operan. J. Bacteriol. 171:53865404.
2. Bardwell, J. C.A., K. McGovern, and J. Beckwith. 1991. Identification of a protein required for disulfide bond formation in vivo. Cell 67:581589.
3. Baudry, B.,, A. Fasano,, J. Ketley,, and J. B. Kaper. 1992. Cloning of a gene (zot) encoding a new toxin produced by Vibrio cholerae. Infect. Immun. 60:428434.
4. Beachey, E. H. 1981. Bacterial adherence: adhesin-receptor interactions mediating the attachment of bacteria to mucosal surfaces. J. Infect. Dis. 143:325345.
5. Bieker, K. L.,, G. J. Phillips,, and T. Silhavy. 1990. The sec and prl genes of Escherichia coli. J. Bioenerg. Biomembr. 22:291310.
5a. Brown, R. C.,, and R. K. Taylor. Unpublished data.
6. DeGraaf, F. K. 1990. Genetics of adhesive fimbriae of intestinal Escherichia coli. Curr. Top. Microbiol. Immunol. 151:2953.
7. DiRita, V. J. 1992. Coordinate expression of virulence genes by ToxR in Vibrio cholerae. Mol. Microbiol. 6:451458.
8. DiRita, V. J.,, C. Parsot,, G. Jander,, and J. J. Mekalanos. 1991. Regulatory cascade controls virulence in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 88:54035407.
9. Doig, P.,, P. A. Sastry,, R. S. Hodges,, K. K. Lee,, W. Paranchych,, and R. T. Irvin. 1990. Inhibition of pilus-mediated adhesion of Pseudomonas aeruginosa to human buccal epithelial cells by monoclonal antibodies directed against pili. Infect. Immun. 58:124130.
10. Donnenberg, M. S.,, J. A. Giron,, J. P. Nataro,, and J. B. Kaper. 1992. A plasmid-encoded type IV fimbrial gene of enteropathogenic Escherichia coli associated with localized adherence. Mol. Microbiol. 6:34273437.
11. Dums, F.,, J. M. Dow,, and M. J. Daniels. 1991. Structural characterization of protein secretion genes of the bacterial phytopathogen Xanthomonas campestris pathovar campes tris: relatedness to secretion systems of other gram-negative bacteria. Mol. Gen. Genet. 229:357364.
12. Dupuy, B.,, M.-K. Taha,, A. P. Pugsley,, and C. Marchai. 1991. Neisseria gonorrhoeae prepilin export studied in Escherichia coli. J. Bacteriol. 173:75897598.
13. Edman, J. C.,, ` Ellis,, R. W. Blacher,, R. A. Roth,, and W. J. Rutter. 1985. Sequence of protein disulfide isomerase and implications of its relationship to thioredoxin. Nature (London) 317:267270.
14. Ehara, M.,, M. Ishibashi,, Y. Ichinose,, M. Iwanaga,, S. Shimodori,, and T. Naito. 1987. Purification and partial characterization of Vibrio cholerae Ol fimbriae. Vaccine 5:283288.
15. Elleman, T. C.,, and R. A. Hoyne. 1984. Nucleotide sequence of the gene encoding pilin of Bacte-roides nodosus, the causal organism of ovine foot-rot. J. Bacteriol. 160:11841187.
16. Ellis, R. J. 1990. The molecular chaperone concept. Semin. Cell Biol. 1:119.
17. Faast, R.,, M. A. Ogierman,, U. H. Stroeher, and R A. Manning. 1989. Nucleotide sequence of the structural gene, tcpA, for a major pilin subunit of Vibrio cholerae. Gene 85:227231.
18. Fasano, A.,, B. Baudry,, D. W. Pumplin,, S. S. Wasserman,, B. D. Tall,, J. M. Ketley,, and J. B. Kaper. 1991. Vibrio cholerae produces a second enterotoxin which affects intestinal tight junctions. Proc. Natl. Acad. Sci. USA. 88:52425246.
19. Finkelstein, R. A.,, M. Bœsman-Finkelstein,, and R. Holt. 1983. Vibrio cholerae hemagglutinin/ lectin/protease hydrolyzes fibronectin and ovomucin: F. M. revisited. Proc. Natl. Acad. Sci. USA 80:10921095.
20. Freedman, R. B. 1984. Native disulfide bond formation in protein biosynthesis: evidence for the role of protein disulfide isomerase. Trends Biochem. Sci. 9:438441.
21. Freedman, R. B.,, N. J. BuUeid,, H. C. Hawkins,, and J. L. Paver. 1989. Role of protein disulfide isomerase in the expression of native proteins. Biochem. Soc. Symp. 55:167192.
22. Fréter, R.,, P. C. M. O'Brien,, and M. S. Macsai. 1981. Role of chemotaxis in the association of motile bacteria with intestinal mucosa: in vivo studies. Infect. Immun. 34:234240.
23. Galen, J. E.,, J. M. Ketley,, A. Fasano,, S. H. Richardson,, S. S. Wasserman,, and J. B. Kaper. 1992. Role of Vibrio cholerae neuraminidase in the function of cholera toxin. Infect. Immun. 60:406415.
24. Giron, J. A.,, A. S. Y. Ho,, and G. K. Schoolnik. 1991. An inducible bundle-forming pilus of entero-pathogenic Escherichia coli. Science 254:710713.
25. Goldberg, M. B.,, V. J. DiRita,, and S. B. Calderwood. 1990. Identification of an iron-regulated virulence determinant in Vibrio cholerae, using TnphoA mutagenesis. Infect. Immun. 58:5560.
26. Haas, I. G.,, and M. Wabl. 1983. Immunoglobulin heavy chain binding protein. Nature (London) 306:387389.
27. Hall, R. H.,, G. Losonsky,, A. P. D. Silveira,, R. K. Taylor,, J. J. Mekalanos,, N. D. Witham,, and M. M. Levine. 1991. Immunogenicity of Vi-brío cholerae O1 toxin coregulated pili in experimental and clinical cholera. Infect. Immun. 59:25082512.
28. Hall, R. H.,, P. A. Vial,, J. B. Kaper,, J. J. Mekalanos,, and M. M. Levine. 1988. Morphological studies on fimbriae expressed by Vibrio cholerae O1. Microb. Pathog. 4:257265.
29. Hanne, L. E.,, and R. A. Finkelstein. 1982. Characterization and distribution of the hemagglutinins produced by Vibrio cholerae. Infect. Immun. 36:209214.
30. Hase, C. C.,, and R. A. Finkelstein. 1991. Cloning and nucleotide sequence of the Vibrio cholerae hemagglutination protease (HA/protease) gene and construction of an HA/protease-negative strain. J. Bacteriol. 173:33113317.
31. Herrington, D. A.,, R. H. Hall,, G. Losonsky,, J. J. Mekalanos,, R. K. Taylor,, and M. M. Levine. 1988. Toxin, toxin-coregulated pili and the toxR regulon are essential for Vibrio cholerae pathogenesis in humans. J. Exp. Med. 168:14871492.
32. Hirst, T. R.,, J. Sanchez,, J. B. Kaper,, S. J. S. Hardy,, and J. Holmgren. 1984. Mechanism of toxin secretion by Vibrio cholerae investigated in strains harboring plasmids that encode heat-labile enterotoxins of Escherichia coli. Proc. Natl. Acad. Sci. USA 81:77527756.
33. Irvin, R. T.,, P. Doig,, K. K. Lee,, P. A. Sastry,, W. Paranchych,, T. Todd,, and R. S. Hodges. 1989. Characterization of the Pseudomonas aeruginosa pilus adhesin: confirmation that the pilin structural protein subunit contains a hyman epithelial cell-binding domain. Infect. Immun. 57:37203726.
34. Jonson, G.,, A. M. Svennerholm,, and J. Holmgren. 1992. Analysis of expression of toxin-coregulated pili in classical and El Tor Vibrio cholerae Ol in vitro and in vivo. Infect. Immun. 60:42784284.
35. Kabir, S.,, N. Ahmad,, and S. Ali. 1984. Neuraminidase production by Vibrio cholerae O1 and other diarrheagenic bacteria. Infect. Immun. 44:747749.
36. Kaufman, M. R.,, J. M. Seyer,, and R. K. Taylor. 1991. Processing of TCP pilin by TcpJ typifies a common step intrinsic to a newly recognized pathway of extracellular protein secretion by gram-negative bacteria. GenesDev. 5:18341846.
37. Kaufman, M. R.,, C. E. Shaw,, I. D. Jones,, and R. K. Taylor. 1993. Biogenesis and regulation of the Vibrio cholerae toxin-coregulated pilus: analogies to other virulence factor secretory systems. Gene 126:4349.
38. Kyte, J.,, and R. F. Doolittle. 1982. A method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105132.
39. Lauer, P.,, N. H. Albertson,, and M. Koomey. 1993. Conservation of genes encoding components of a type IV pilus assembly-two-step protein export pathway in Neisseria gonorrhoeae. Mol. Microbiol. 8:357368.
40. Manoil, C.,, and J. Beckwith. 1985. TnphoA : a transposon probe for protein export signals. Proc. Natl. Acad. Sci. USA 82:81298133.
41. Marrs, C.,, G. Schoolnik,, J. M. Koomey,, J. Hardy,, J. Rothbard,, and S. Falkow. 1985. Cloning and sequencing of a Moraxella bovis pilin gene. J. Bacteriol. 163:132139.
42. Mekalanos, J. J.,, R. J. Collier,, and W. R. Romig. 1977. Simple method for purifying chol-eragenoid, the natural toxoid of Vibrio cholerae. Infect. Immun. 16:789795.
43. Meng, M.,, and H. P. C.. Hogenkamp. 1981. Purification, characterization, and amino acid sequence of thioredoxin from Corynebacterium nephridii. J. Biol. Chem. 256:91749182.
44. Meyer, T. F.,, E. Billyard,, R. Haas,, S. Storzbach,, and M. So. 1984. Pilus genes of Neisseria gonorrheal, chromosomal organization and DNA sequence. Proc. Natl. Acad. Sci. USA 81:61106114.
45. Michiels, T.,, and G. R. Cornells. 1991. Secretion of hybrid proteins by the Yersinia Yop export system. J. Bacteriol. 173:16771685.
46. Michiels, T.,, J.-C. Vanooteghem,, C. Lambert De Rouvriot,, B. China,, A. Gustin,, P. Boudry,, and G. R. Cornells. 1991. Analysis of virC, an operon involved in the secretion of Yop proteins by Yersinia entercolitica. J. Bacteriol. 173:49945009.
47. Miller, V. L.,, and J. J. Mekalanos. 1984. Synthesis of cholera toxin is positively regulated at the transcriptional level by toxR. Proc. Natl. Acad. Sci. USA 81:34713475.
48. Miller, V. L.,, R. K. Taylor,, and J. J. Mekalanos. 1987. Cholera toxin transcriptional activator ToxR is a transmembrane DNA binding protein. Cell 48:271279.
49. Nunn, D. N.,, and S. Lory. 1991. Product of the Pseudomonas aeruginosa gene pilD is a prepilin leader peptidase. Proc. Natl. Acad. Sci. USA 88:32813285.
50. O'Brien, A. D.,, M. E. Chen,, R. K. Holmes,, J. Kaper,, and M. M. Levine. 1984. Environmental and human isolates of Vibrio cholerae and Vibrio parahaemolyticus produce a Shigella dysenteriae 1 (Shiga)-like cytotoxin. Lancet. 1:7778.
51. Ogata, R. T.,, C. Winters,, and R. P. Levine. 1982. Nucleotide sequence analysis of the complement resistance gene from plasmid R100. J. Bacteriol. 151:819827.
52. Ogierman, M. A.,, S. Zabihi,, L. Mourtzios,, and P. A. Manning. 1993. Genetic organization and sequence of the promoter-distal region of the tcp gene cluster of Vibrio cholerae. Gene 126:5160.
53. Oliver, D. 1985. Protein secretion in Escherichia coli. Annu. Rev. Microbiol. 39:615648.
54. Paranchych, W.,, and L. S. Frost. 1988. The physiology and biochemistry of pili. Adv. Microb. Physiol. 29:53114.
55. Parsot, C.,, E. Taxman,, and J. J. Mekalanos. 1991. ToxR regulates the production of lipoproteins and the expression of serum resistance in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 88:16411645.
56. Pasloske, B. L.,, and W. Parancych. 1988. The expression of mutant pilins in Pseudomonas aeruginosa: fifth position glutamate affects pilin methylation. Mol. Microbiol. 2:489495.
57. Peek, J. A.,, and R. K. Taylor. 1992. Characterization of a periplasmic thiol disulfide interchange protein required for the functional maturation of secreted virulence factors of Vibrio cholerae. Proc. Natl. Acad. Sci. USA 89:62106214.
57a. Peek, J. A.,, and R. K. Taylor. Submitted for publication.
58. Perumal, N. B.,, and E. G. J. Minkley. 1984. The product of the F sex factor traT surface exclusion gene is a lipoprotein. J. Biol. Chem. 259:53575360.
59. Peterson, K. M.,, and J. J. Mekalanos. 1988. Characterization of the Vibrio cholerae ToxR regu-lon: identification of novel genes involved in intestinal colonization. Infect. Immun. 56:28222829.
60. Pugsley, A. P. 1993. The complete general secretory pathway in gram-negative bacteria. Microbiol. Rev. 57:50108.
61. Rhen, M.,, and S. Sukupolvi. 1988. The role of the traT gene of the Salmonella typhimurium virulence plasmid for serum resistance and growth within liver macrophages. Microb. Pathog. 5:275285.
61a. Rhine, J. A.,, and R. K. Taylor. Submitted for publication.
62. Rothbard, J. B.,, R. Fernandez,, L. Wang,, N. N. H. Teng,, and G. K. Schoolnik. 1985. Antibodies to peptides corresponding to a conserved sequence of gonococcal pilins block bacterial adhesion. Proc. Natl. Acad. Sci. USA 82:915919.
63. Ruoslahti, E. 1988. Fibronectin and its receptors. Annu. Rev. Biochem. 57:375413.
64. Ruoslahti, E., and M. D. Pierschbacher. 1987. New perspectives in cell adhesion: RGD and integrine. Science 238:491497.
65. Russel, M. 1991. Filamentous phage assembly. Mol. Microbiol. 5:16071613.
66. Ruvkun, G. B.,, and F. M. Ausubel. 1981. A general method for site-directed mutagenesis in prokaryotes. Nature (London) 289:8588.
67. Sastry, P. A.,, J. R. Pearlstone,, L. B. Smillie,, and W. Paranchych. 1983. Amino acid sequence of pilin isolated for Pseudomonas aeruginosa PAK. FEBS Lett. 151:253256.
68. Schatz, P.,, and J. Beckwith. 1990. Genetic analysis of protein export in Escherichia coli. Annu. Rev. Genet. 24:215248.
69. Schoolnik, G. K.,, R. Fernandez,, J. Y. Tai,, J. Rothbard,, and E. C. Gotschlich. 1984. Gonococcal pili: primary structure and receptor binding domain. J. Exp. Med. 159:13511370.
70. Sharma, D. P.,, C. Thomas,, R. H. Hall,, M. M. Levine,, and S. R. Attridge. 1989. Significance of toxin-coregulated pili as protective antigens of Vibrio cholerae on the infant mouse model. Vaccine 7:451456.
71. Shaw, C. E.,, K. M. Peterson,, J. J. Mekalanos,, and R. K. Taylor,. 1990. Genetic studies of Vibrio cholerae TCP pilus biogenesis, p. 5158. In R. B. Sack, and Y. Zinnaka (ed.), Advances in Research on Cholera and Related Diarrheas, vol. 7. KTK Scientific Publishers, Tokyo.
72. Shaw, C. E.,, K. M. Peterson,, D. Sun,, J. J. Mekalanos,, and R. K. Taylor,. 1988. TCP pilus expression and biogenesis by classical and El Tor biotypes of Vibrio cholerae Ol, p. 2335. In Switalski,, Hook,, and Beachey (ed.), Molecular Mechanisms of Microbial Adhesion. Springer-Verlag, New York.
73. Shaw, C. E.,, and R. K. Taylor. 1990. Vibrio cholerae 0395 tcpA pilin gene sequence and comparison of predicted protein structural features to those of type 4 pilins. Infect. Immun. 58:30423049.
74. Strom, M. A.,, and S. Lory. 1987. Mapping of export signals of Pseudomonas aeruginosa pilin with alkaline phosphatase fusions. J. Bacteriol. 169:31813188.
75. Strom, M. S.,, and S. Lory. 1991. Amino acid substitutions in pilin of Pseudomonas aeruginosa: effect on leader peptide cleavage, amino-terminal methylation, and pilus assembly. J. Biol. Chem. 266:16561664.
76. Sun, D.,, J. J. Mekalanos,, and R. K. Taylor. 1990. Antibodies directed against the toxin-coregulated pilus from Vibrio cholerae provide protection in the infant mouse experimental cholera model. J. Infect. Dis. 161:12311236.
77. Sun, D.,, J. M. Sever,, I. Kovari,, R. A. Sumrada,, and R. K. Taylor. 1991. Localization of protective epitopes within the pilin subunit of the Vibrio cholerae toxin-coregulated pilus. Infect. Immun. 59:114118.
78. Sun, D.,, D. M. Tillman,, T. N. Marion,, and R. K. Taylor. 1990. Production and characterization of monoclonal antibodies to the toxin coregulated pilus (TCP) of Vibrio cholerae that protect against experimental cholera in infant mice. Serodiagn. Immunother. Infect. Dis. 4:7381.
79. Taylor, R.,, C. Shaw,, K. Peterson,, P. Spears,, and J. Mekalanos. 1988. Safe live Vibrio cholerae vaccines? Vaccine 6:151154.
80. Taylor, R. K.,, C. Manoil,, and J. J. Mekalanos. 1989. Broad host-range vectors for delivery of TnphoA: use in genetic analysis of secreted virulence determinants of Vibrio cholerae. J. Bacteriol. 171:18701878.
81. Taylor, R. K.,, V. L. Miller,, D. B. Furlong,, and J. J. Mekalanos. 1987. The use of phoA gene fusions to identify a pilus colonization factor coordinate^ regulated with cholera toxin. Proc. Natl. Acad. Sci. USA 84:28332837.
82. Thayer, M. M.,, K. M. Flaherty,, and D. B. McKay. 1991. Three dimensional structure of the elastase of Pseudomonas aeruginosa at 1.5A resolution. J. Biol. Chem. 266:28642871.
83. Tomb, J. F. 1992. A periplasmic protein disulfide oxidoreductase is required for transformation of Haemophilus influenzae Rd. Proc. Natl. Acad. Sci. USA 89:1025210256.
84. von Heijne, G. 1985. Signal sequences: the limits of variation. J. Mol. Biol. 184:99105.
85. Wickner, W.,, A. J. M. Driessen,, and F.-U. Hartl. 1991. The enzymology of protein translocation across the Escherichia coli plasma membrane. Annu. Rev. Biochem. 60:101124.
86. Yu, J.,, H. Webb,, and T. R. Hirst. 1992. A homologue of the Escherichia coli DsbA protein involved in disulfide bond formation is required for enterotoxin biogenesis in Vibrio cholerae. Mol. Microbiol. 6:19491958.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error