Secretion of proteins and assembly of bacterial surface organelles: Shared pathways of extracellular protein targeting

Current Opinion in Microbiology

Volumn 1, Issue 1, 1998, Pages 27-35

  Lory, Stephen ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); NEGIBACTERIA;

BACTERIAL PROTEIN; MEMBRANE PROTEIN;

CELL ORGANELLE; GENE EXPRESSION REGULATION; GENETICS; GRAM NEGATIVE BACTERIUM; METABOLISM; MOLECULAR EVOLUTION; PATHOGENICITY; PROTEIN FOLDING; REVIEW; VIRULENCE;

BACTERIAL PROTEINS; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, BACTERIAL; GRAM-NEGATIVE BACTERIA; MEMBRANE PROTEINS; ORGANELLES; PROTEIN FOLDING; VIRULENCE;

EID: 0031988031     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1369-5274(98)80139-2     Document Type: Article

References (71)

1. Salmond GP, Reeves PJ: Membrane traffic wardens and protein secretion in Gram-negative bacteria. Trends Biochem Sci 1993, 18:7-12.
2. Winans SC, Burns DL, Christie PJ: Adaptation of a conjugal transfer system for the export of pathogenic macromolecules. Trends Microbiol 1996, 4:64-68.
3. Klauser T, Pohlner J, Meyer TF: The secretion pathway of IgA protease-type proteins in Gram-negative bacteria. Bioessays 1993, 15:799-805.
4. Binet R, Létoffé S, Ghigo JM, Delepelaire P, Wandersman C: Protein secretion by Gram negative bacterial ABC exporters: a review. Gene 1997, 192:7-11.
5. Zhang LH, Path MJ, Mahanty HK, Tai PC, Kolter R: Genetic analysis of the colicin V secretion pathway. Genetics 1995, 141:25-32.
6. Path MJ, Kolter R: ABC transporters: bacterial exporters. Microbiol Rev 1993, 57:995-1017.
7. Wandersman C, Delepelaire P: TolC, an Escherichia coli outer membrane protein required for hemolysin secretion. Proc Natl Acad Sci USA 1990, 87:4776-4780.
8. Dinh T, Paulsen IT, Saier MH Jr: A family of extracytoplasmic proteins that allow transport of large molecules across the outer membranes of Gram negative bacteria. J Bacteriol 1994, 176:3825-3831.
9. Pugsley AP: The complete general secretory pathway in Gram-negative bacteria. Microbiol Rev 1993, 57:50-108.
10. Menard R, Dehio C, Sansonetti PJ: Bacterial entry into epithelial cells: the paradigm of Shigella. Trends Microbiol 1996, 4:220-226.
11. Galan JE: Molecular genetic bases of Salmonella entry into host cells. Mol Microbiol 1996, 20:263-271.
12. Cornelis GR, Wolf-Watz H: The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells. Mol Microbiol 1997, 23:861-867.
13. Lee CA: Type III secretion systems: machines to deliver bacterial proteins into eukaryotic cells? Trends Microbiol 1997, 5:148-156.
14. Yahr TL, Goranson J, Frank DW: Exoenzyme S of Pseudomonas aeruginosa is secreted by a type III pathway. Mol Microbiol 1996, 22:991-1003.
15. Baker B, Zambryski P, Staskawicz B, Dinesh-Kumar SP: Signaling in plant microbe interactions. Science 1997, 276:726-733.
16. Weiss AA, Johnson FD, Burns DL: Molecular characterization of an operon required for pertussis toxin secretion. Proc Natl Acad Sci USA 1993, 90:2970-2974.
17. Tummuru MK, Sharma SA, Blaser MJ: Helicobacter pylori picB, a homologue of the Bordetella pertussis toxin secretion protein, is required for induction of IL 8 in gastric epithelial cells. Mol Microbiol 1995, 18:867-876.
18. Strom MS, Lory S: Structure function and biogenesis of the type IV pili. Annu Rev Microbiol 1993, 47:565-596.
19. Nunn DN, Lory S: Product of the Pseudomonas aeruginosa gene pilD is a prepilin leader peptidase. Proc Natl Acad Sci USA 1991, 88:3281-3285.
20. Strom MS, Nunn DN, Lory S: A single bifunctional enzyme, PilD, catalyzes cleavage and N-methylation of proteins belonging to the type IV pilin family. Proc Natl Acad Sci USA 1993, 90:2404-2408.
21. Lu HM, Motley ST, Lory S: Interactions of the components of the general secretion pathways: role of Pseudomonas aeruginosa type IV pilin subunits in complex formation and extracellular secretion. Mol Microbiol 1997, 25:247-259.
22. Rudel T, Scheurerpflug I, Meyer TF: Neisseria PilC protein identified as type 4 pilus tip located adhesin. Nature 1995, 373:357-359.
23. Alm RA, Hallinan JP, Watson AA, Mattick JS: Fimbrial biogenesis genes of Pseudomonas aeruginosa: pilW and pilX increase the similarity of type 4 fimbriae to the GSP protein secretion systems and pilY1 encodes a gonococcal PilC homologue. Mol Microbiol 1996, 22:161-173.
24. Gough CL, Genin S, Zischek C, Boucher CA: hrp genes of Pseudomonas solanacearum are homologous to pathogenicity determinants of animal pathogenic bacteria and are conserved among plant pathogenic bacteria. Mol Plant Microbe Interact 1992, 5:384-389.
25. Aizawa SI: Flagellar assembly in Salmonella typhimurium. Mol Microbiol 1996, 19:1-5.
26. Hughes KT, Gillen KL, Semon MJ, Karlinsey JE: Sensing structural intermediates in bacterial flagellar assembly by export of a negative regulator. Science 1993, 262:1277-1280.
27. An F, Macnab RM: Enzymatic characterization of Flil An ATPase involved in flagellar assembly in Salmonella typhimurium. J Biol Chem 1996, 271:31981-31988.
28. Ginocchio CC, Olmsted SB, Wells CL, Gal'an JE: Contact with epithelial cells induces the formation of surface appendages on Salmonella typhimurium. Cell 1994, 76:717-724.
29. Michiels T, Wattiau P, Brasseur R, Ruysschaert J M, Cornelis G; Secretion of Yop proteins by Yersiniae. Infect Immun 1990, 58:2840-2849.
30. Parsot C, Menard R, Gounon P, Sansonetti PJ: Enhanced secretion through the Shigella flexneri Mxi Spa translocon leads to assembly of extracellular proteins into macromolecular structures. Mol Microbiol 1995, 16:291-300.
31. Roine E, Wei W, Yuan J, Nurmiaho Lassila E, Kalkkinen N, Romantschuk M, He SY: Hrp pilus: an hrp dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci USA 1997, 94:3459-3464.
32. Tomb JF, White O, Kerlavage AR, Clayton RA, Sutton GG, Fleischmann RD, Ketchum KA, Klenk HP, Gill S, Dougherty BA et al.: The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 1997, 388:539-547.
33. Ward JE, Akiyoshi DE, Regier D, Datta A, Gordon MP, Nester EW: Characterization of the virB operon from an Agrobacterium tumefaciens Ti plasmid. J Biol Chem 1988, 263:5804-5814.
34. Bundock P, den Dulk-Ras A, Beijersbergen A, Hooykaas PJ: Trans kingdom T DNA transfer from Agrobacterium tumefaciens to Saccharomyces cerevisiae. EMBO J 1995, 14:3206-3214.
35. Covacci A, Rappuoli R: Pertussis toxin export requires accessory genes located downstream from the pertussis toxin operon. Mol Microbiol 1993, 8:429-434.
36. Kotob SI, Hausman SZ, Burns DL: Localization of the promoter for the ptl genes of Bordetella pertussis, which encode proteins essential for secretion of pertussis toxin. Infect Immun 1995, 63:3227-3230.
37. Pizza M, Bugnoli M, Manetti R, Covacci A, Rappuoli R: The subunit S1 is important for pertussis toxin secretion. J Biol Chem 1990, 265:17759-17763.
38. Christie PJ: Agrobacterium tumefaciens T complex transport apparatus: paradigm for a new family of multifunctional transporters in eubacteria. J Bacteriol 1997, 179:3085-3094.
39. Fullner KJ, Lara JC, Nester EW: Pilus assembly by Agrobacterium T DNA transfer genes. Science 1996, 273:1107-1109.
40. Mackman N, Baker K, Gray L, Haigh R, Nicaud JM, Holland IB: Release of a chimeric protein into the medium from Escherichia coli using the C terminal secretion signal of haemolysin. EMBO J 1987, 6:2835-2841.
41. Delepelaire P, Wandersman C: Protein secretion in Gram negative bacteria. The extracellular metalloprotease B from Erwinia chrysanthemi contains a C terminal secretion signal analogous to that of Escherichia coli alpha hemolysin. J Biol Chem 1990, 265:17118-17125.
42. Létoffé S, Wandersman C: Secretion of CyaA PrtB and HlyA PrtB fusion proteins in Escherichia coli: involvement of the glycine rich repeat domain of Erwinia chrysanthemi protease B. J Bacteriol 1992, 174:4920-4927.
43. Chervaux C, Holland IB: Random and directed mutagenesis to elucidate the functional importance of helix II and F 989 in the C terminal secretion signal of Escherichia coli hemolysin. J Bacteriol 1996, 178:1232-1236.
44. Ghigo JM, Wandersman C: A carboxyl terminal four amino acid motif is required for secretion of the metalloprotease PrtG through the Erwinia chrysanthemi protease secretion pathway. J Biol Chem 1994, 269:8979-8985.
45. Sauvonnet N, Pugsley AP: Identification of two regions of Klebsiella oxytoca pullulanase that together are capable of promoting beta lactamase secretion by the general secretory pathway. Mol Microbiol 1996, 22:1-7.
46. Lu HM, Lory S: A specific targeting domain in mature exotoxin A is required for its extracellular secretion from Pseudomonas aeruginosa. EMBO J 1996, 15:429-436.
47. McVay CS, Hamood AN: Toxin A secretion in Pseudomonas aeruginosa: the role of the first 30 amino acids of the mature toxin. Mol Gen Genet 1995, 249:515-525.
48. Wattiau P, Woestyn S, Cornelis GR: Customized secretion chaperones in pathogenic bacteria. Mol Microbiol 1996, 20:255-262.
49. Sory MP, Boland A, Lambermont I, Cornells GR: Identification of the YopE and YopH domains required for secretion and internalization into the cytosol of macrophages, using the cyaA gene fusion approach. Proc Natl Acad Sci USA 1995, 92:11998-12002.
50. Cheng LW, Anderson DM, Schneewind O: Two independent type III secretion mechanisms for YopE in Yersinia enterocolitica. Mol Microbiol 1997, 24:757-765. A surprising discovery of a second targeting signal in a protein secreted by the Type III secretion pathway. The signal functions only in the presence of the cognate chaperone, This suggests a possible role for the secretion chaperones in targeting as well as in maintenance of secretion competence of the Yop proteins.
51. Kuwajima G, Kawagishi I, Homma M, Asaka J, Kondo E, Macnab RM: Export of an N terminal fragment of Escherichia coli flagelli by a flagellum specific pathway. Proc Natl Acad Sci USA 1989, 86:4953-4957.
52. Kornacker MG, Newton A: Information essential for cell cycle dependent secretion of the 591 residue Caulobacter hook protein is confined to a 21 amino acid sequence near the N terminus. Mol Microbiol 1994, 14:73-85.
53. McIver KS, Kessler E, Olson JC, Ohman DE: The elastase propeptide functions as an intramolecular chaperone required for elastase activity and secretion in Pseudomonas aeruginosa. Mol Microbiol 1995, 18:877-889.
54. Braun P, Tommassen J, Filloux A: Role of the propeptide in folding and secretion of elastase of Pseudomonas aeruginosa. Mol Microbiol 1996, 19:297-306. This paper, along with McIver et al. [53], used an approach that demonstrated that domains in secreted proteins can function as intramolecular customized chaperones. This work has broad implications for trafficking of a class of enzymes synthesized with transient prepeptides, where these peptides may function as chaperones for protein secretion.
55. Frenken LG, de Groot A, Tommassen J, Verrips CT: Role of the lipB gene product in the folding of the secreted lipase of Pseudomonas glumae. Mol Microbiol 1993, 9:591-599.
56. Wattiau P, Cornelis GR: SycE, a chaperone like protein of Yersinia enterocolitica involved in the secretion of YopE. Mol Microbiol 1993, 8:123-131.
57. Woestyn S, Sory MP, Boland A, Laquenne O, Cornells GR: The cytosolic SycE and SycH chaperones of Yersinia protect the region of YopE and YopH involved in in translocation across eukaryotic cell membranes. Mol Microbiol 1996, 20:1 261-1271.
58. Wattiau P, Bernier B, Desl'ee P, Michiels T, Cornelis GR: Individual chaperones required for Yop secretion by Yersinia. Proc Natl Acad Sci USA 1994, 91:10493-10497.
59. Menard R, Sansonetti P, Parsot C, Vasselon T: Extracellular association and cytoplasmic partitioning of the IpaB and IpaC invasins of S. flexneri. Cell 1994, 79:515-525.
60. Kaniga K, Tucker S, Trollinger D, Gal'an JE: Homologs of the Shigella IpaB and IpaC invasins are required for Salmonella typhimurium entry into cultured epithelial cells. J Bacteriol 1995, 177:3965-3971.
61. Buchner J: Supervising the fold: functional principles of molecular chaperones. FASEB J 1996, 10:1-9.
62. Hardie KR, Lory S, Pugsley AP: Insertion of an outer membrane protein in Escherichia coli requires a chaperone like protein. EMBO J 1996, 15:978-988.
63. Drake SL, Sandstedt SA, Koomey M: PilP, a pilus biogenesis lipoprotein in Neisseria gonorrhoeae. Mol Microbiol 1997, 23:657-668.
64. Daefler S, Guilvout I, Hardie KR, Pugsley AP, Russel M: The C terminal domain of the secretin PulD contains the binding site for its cognate chaperone, PulS, and confers PulS dependence on plVf1 function. Mol Microbiol 1997, 24:465-475. An elegant study demonstrating specific interactions of a chaperone lipoprotein, PulS, with its substrate, PulD, a putative outer membrane channel for secretion of proteins across the outer membrane. The authors map the PulS-binding domain of PulD to its carboxyl terminus and use gene fusions to show that a passenger outer membrane protein assembles if it is supplied with PulS. This work suggests that customized chaperone-like activities, most likely carried out by lipoproteins, are for proper localization and function of all proteins related to PulD, which is the member of the GspD family of proteins found in both Type II and Type III secretion machineries.
65. Wengelnik K, Marie C, Russel M, Bonas U: Expression and localization of HrpA1, a protein of Xanthomonas campestris pv. vesicatoria essential for pathogenicity and induction of the hypersensitive reaction. J Bacteriol 1996, 178:1061-1069.
66. Plano GV, Straley SC: Mutations in yscC, yscD, and yscG prevent high level expression and secretion of V antigen and Yops in Yersinia pestis. J Bacteriol 1995, 177:3843-3854.
67. Anderson LB, Hertzel AV, Das A: Agrobacterium tumefaciens VirB7 and VirB9 form a disulfide linked protein complex. Proc Natl Acad Sci USA 1996, 93:8889-8894.
68. Fernandez D, Spudich GM, Zhou XR, Christie PJ: The Agrobacterium tumefaciens VirB7 lipoprotein is required for stabilization of VirB proteins during assembly of the T complex transport apparatus. J Bacteriol 1996, 178:3168-3176.
69. Spudich GM, Fernandez D, Zhou XR, Christie PJ: Intermolecular disulfide bonds stabilize VirB7 homodimers and VirB7/VirB9 heterodimers during biogenesis of the Agrobacterium tumefaciens T complex transport apparatus. Proc Natl Acad Sci USA 1996, 93:7512-7517.
70. Farizo KM, Cafarella TG, Burns DL: Evidence for a ninth gene, ptII, in the locus encoding the pertussis toxin secretion system of Bordetella pertussis and formation of a PtII PtIF complex. J Biol Chem 1996, 271:31643-31649.
71. Pugsley AP, Chapon C, Schwartz M: Extracellular pullulanase of Klebsiella pneumoniae is a lipoprotein. J Bacteriol 1986, 166:1083-1088.