Biochemistry of type IV secretion

Current Opinion in Microbiology

Volumn 2, Issue 1, 1999, Pages 25-29

  Burns, Drusilla L ^a  

^a CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; BACTERIAL TOXIN; DNA; PERTUSSIS TOXIN;

ARTICLE; BACTERIUM PILUS; BORDETELLA PERTUSSIS; COMPLEX FORMATION; DNA TRANSFER; GRAM NEGATIVE BACTERIUM; HELICOBACTER PYLORI; INTERNALIZATION; LEGIONELLA PNEUMOPHILA; MACROMOLECULE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RHIZOBIUM RADIOBACTER; SEQUENCE HOMOLOGY; STRUCTURE ANALYSIS;

AGROBACTERIUM TUMEFACIENS; BACTERIA (MICROORGANISMS); BORDETELLA PERTUSSIS; HELICOBACTER PYLORI; LEGIONELLA PNEUMOPHILA; NEGIBACTERIA;

EID: 0032996225     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1369-5274(99)80004-6     Document Type: Article

References (53)

1. Zambryski P Basic processes underlying Agrobacterium-mediated DNA transfer to plant cells. Annu Rev Genet. 22:1988;1-30.
2. Zambryski P Chronicles from the Agrobacterium-plant cell DNA transfer story. Annu Rev Plant Physiol Plant Mol Biol. 43:1992;465-490.
3. Berger BR, Christie PJ Genetic complementation analysis of the Agrobacterium tumefaciens virB2 through virB11 are essential virulence genes. J Bacteriol. 176:1994;3646-3660.
4. Fullner KJ Role of Agrobacterium virB genes in transfer of T complexes and RSF1010. J Bacteriol. 180:1998;430-434.
5. Otten L, De Greve H, Leemans J, Hain R, Hooykaas P, Schell J Restoration of virulence of vir region mutants of Agrobacterium strains. Mol Gen Genet. 195:1984;159-163.
6. Binns AN, Beaupre CE, Dale EM Inhibition of VirB-mediated transfer of diverse substrates from Agrobacterium tumefaciens by the IncQ plasmid RSF1010. J Bacteriol. 177:1995;4890-4899.
7. Regensburg-Tuink AJG, Hooykaas PJJ Transgenic N. glauca plants expressing bacterial virulence gene virF are converted into hosts for nopaline strains of A. tumefaciens. Nature. 363:1993;69-71.
8. Citovsky V, Zupan J, Warnick D, Zambryski P Nuclear localization of Agrobacterium VirE2 protein in plant cells. Science. 256:1992;1802-1805.
9. Beijersbergen A, Den Dulk-Ras A, Schilperoort RA, Hooykaas PJJ Conjugative transfer by the virulence system of Agrobacterium tumefaciens. Science. 256:1992;1324-1327.
10. Bohne J, Yim A, Binns AN The Ti plasmid increases the efficiency of Agrobacterium tumefaciens as a recipient in virB-mediated conjugal transfer of an IncQ plasmid. Proc Natl Acad Sci USA. 95:1998;7057-7062. This report demonstrates that Agrobacterium-to-Agrobacterium transfer efficiencies of the IncQ plasmid RSF1010 increase if the recipient strain, in addition to the donor strain, produces a subset of the VirB proteins. Because only a subset of the VirB proteins are required to increase the efficiency of import of DNA, it may be possible to study functional aspects of a simplified version of the transport complex.
11. Haase J, Lurz R, Grahn AM, Bamford DH, Lanka E Bacterial conjugation mediated by plasmid RP4: RSF1010 mobilization, donor-specific pahge propagation, and pilus production require the same Tra2 core components of a proposed DNA transport complex. J Bacteriol. 177:1995;4779-4791.
12. Lessl M, Balzer D, Pansegrau W, Lanka E Sequence similarities between the RP4 Tra2 and the Ti VirB region strongly support the conjugation model for T-DNA transfer. J Biol Chem. 267:1992;20471-20480.
13. Pohlman RF, Genetti HD, Winans SC Common ancestry between IncN conjugal transfer genes and macromolecular export systems of plant and animal pathogens. Mol Microbiol. 14:1994;655-668.
14. Weiss AA, Johnson FD, Burns DL Molecular characterization of an operon required for pertussis toxin secretion. Proc Natl Acad Sci USA. 90:1993;2970-2974.
15. Covacci A, Rappuoli R Pertussis toxin export requires accessory genes located downstream from the pertussis toxin operon. Mol Microbiol. 8:1993;429-434.
16. Covacci A, Falkow S, Berg DE, Rappuoli R Did the inheritance of a pathogenicity island modify the virulence of Helicobacter pylori? Trends Microbiol. 5:1997;205-208. The authors note that the H. pylori chromosome contains four genes that are predicted to encode proteins that exhibit striking homology to members of type IV transport systems extending the type IV family of proteins to another human pathogen.
17. Tummuru MKR, 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. 18:1995;867-876.
18. Vogel JP, Andrews HL, Wong SK, Isberg RR Conjugative transfer by the virulence system of Legionella pneumophila. Science. 279:1998;873-876. The type IV family of proteins was further expanded when genes encoding type IV homologues were discovered in L. pneumophila. Although the function of these homologues remains unknown, they were shown to be able to play a role in the transfer of DNA between bacteria.
19. ••], these authors reported that L. pneumophila contained genes encoding type IV transporter homologues that appeared to be part of a complex that was capable of transporting DNA from bacteria to bacteria. The actual function of this system of proteins remains obscure.
20. Baron C, Llosa M, Zhou S, Zambryski PC VirB1, a component of the T-complex transfer machinery of Agrobacterium tumefaciens, is processed to a C-terminal secreted product, VirB1*. J Bacteriol. 179:1997;1203-1210. Our knowledge of the architecture of type IV transporters was extended when it was found that a processed from of VirB1 is exported from the bacterial cell and associates with the VirB9-VirB7 heterodimer.
21. Beijersbergen A, Smith SJ, Hooykaas PJJ Localization and topology of VirB proteins of Agrobacterium tumefaciens. Plasmid. 32:1993;212-218.
22. Fernandez D, Dang TAT, Spudich GM, Zhou X-R, Berger B, Christie PJ The Agrobacterium tumefaciens virB7 gene product, a proposed component of the T-complex transport apparatus, is a membrane-associated lipoprotein exposed at the periplasmic surface. J Bacteriol. 178:1996;3156-3167.
23. Fullner KJ, Lara JC, Nester EW Pilus assembly by Agrobacterium T-DNA transfer genes. Science. 273:1996;1107-1109.
24. Lai E-M, Kado CI Processed VirB2 is the major subunit of the promiscuous pilus of Agrobacterium tumefaciens. J Bacteriol. 180:1998;2711-2727. The earlier exciting finding that a pilus is associated with the VirB transport machinery was further extended with this report in which the authors identified the major subunit of the pilus as being VirB2.
25. Dang TAT, Christie PJ The VirB4 ATPase of Agrobacterium tumefaciens is a cytoplasmic membrane protein exposed at the periplasmic surface. J Bacteriol. 179:1997;453-462. VirB4 is likely to play a critical role in the transport process and therefore knowledge of its membrane morphology is an important step in discerning its function. By fusing VirB4 to alkaline phosphatase lacking a signal sequence, the authors were able to elucidate the membrane topology of this protein. From these data, VirB4 appears to be an integral cytopalsmic membrane protein with two periplasmic domains.
26. Thorstenson YR, Kuldau GA, Zambryski PC Subcellular localization of seven VirB proteins of Agrobacterium tumefaciens: implications for the formation of a T-DNA transport structure. J Bacteriol. 176:1993;5233-5241.
27. Ward JE, Dale EM, Nester EW, Binns AN Identification of a VirB10 protein aggregate in the inner membrane of Agrobacterium tumefaciens. J Bacteriol. 172:1990;5200-5210.
28. Das A, Xie Y-H Construction of transposon Tn3phoA: its application in defining the membrane topology of the Agrobacterium tumefaciens DNA transfer proteins. Mol Microbiol. 27:1998;405-414. The authors use VirB/alkaline phosphatase fusions to discern the membrane topology of a number of the VirB proteins. Previous work has studied the topology of these proteins when expressed in E. coli. This work, for the first time, examines topology of these proteins in Agrobacterium.
29. Christie PJ, Ward JE, Gordon MP, Nester EW A gene required for tranfer of T-DNA to plants encodes an ATPase with autophosphorylating activity. Proc Natl Acad Sci USA. 86:1989;9677-9681.
30. Baron C, Thorstenson YR, Zambryski PC The lipoprotein VirB7 interacts with VirB9 in the membranes of Agrobacterium tumefaciens. J Bacteriol. 179:1997;1211-1218. The yeast two-hybrid system was used to visualize the interaction between VirB9 and VirB7, which represents one of the first successful uses of this assay system to define the interactions between membrane proteins.
31. Fernandez D, Spucich GM, Zhou X-R, Christie PJ The Agrobacterium tumefaciens VirB7 lipoprotein is required for stabilization of VirB proteins during assembly of the T-complex transport apparatus. J Bacteriol. 178:1996;3168-3176.
32. Spudich GM, Fernandez D, Zhou Z-R, 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. 93:1996;7512-7517.
33. Anderson LB, Hertzel AV, Das A Agrobacterium tumefaciens VirB7 and VirB9 form a disulfide-linked protein complex. Proc Natl Acad Sci USA. 93:1996;8889-8894.
34. Beaupre CE, Bohne J, Dale EM, Binns AN Interactions between VirB9 and VirB10 membrane proteins involved in movement of DNA from Agrobacterium tumefaciens into plant cells. J Bacteriol. 179:1997;78-89. VirB9 is essential for VirB10 to participate in higher molecular weight complexes suggesting that VirB9 may either directly or indirectly interact with VirB10, providing additional evidence for the existence of a relatively large transport apparatus.
35. Jones AL, Shirasu K, Kado CI The prouduct of the virB4 gene of Agrobacterium tumefaciens promotes accumulation of VirB3 protein. J Bacteriol. 176:1994;5255-5261.
36. Zhou Z-R, Christie PJ Suppression of mutant phenotypes of the Agrobacterium tumefaciens VirB11 ATPase by overproduction of VirB proteins. J Bacteriol. 179:1997;5835-5842. This report demonstrates that the VirB transporter contains more than one VirB11 subunit and that VirB11 interacts with VirB9 and VirB10 during transporter biogenesis, providing additional evidence that the transporter may be a large apparatus.
37. Jones AL, Lai E-M, Shirasu K, Kado CI VirB2 is a processed pilin-like protein encoded by the Agrobacterium tumefaciens Ti plasmid. J Bacteriol. 178:1996;5706-5711.
38. Farizo KM, Cafarella TG, Burns DL Evidence for a ninth gene, ptlI, in the locus encoding the pertussis toxin secretion system of Bordetella pertussis and formation of a PtlI-PtlF complex. J Biol Chem. 271:1996;31643-31649.
39. Cellini C, Kalogeraki S, Winans SC The hydrophobic TraM protein of pKM101 is required for conjugal transfer and sensitivity to donor-specific bacteriophage. Plasmid. 37:1997;181-188.
40. Rashkova S, Spudich GM, Christie PJ Characterization of membrane and protein interaction determinants of the Agrobacterium tumefaciens VirB11 ATPase. J Bacteriol. 179:1997;583-591.
41. Stephens KM, Roush C, Nester E Agrobacterium tumefaciens VirB11 protein requires a consensus nucleotide-binding site for function in virulence. J Bacteriol. 177:1995;27-36.
42. Fullner KJ, Stephens KM, Nester EW An essential virulence protein of Agrobacterium tumefaciens, VirB4, requires an intact mononucleotide binding domain to function in transfer of T-DNA. Mol Gen Genet. 245:1994;704-715.
43. Berger BR, Christie PJ The Agrobacterium tumefaciens virB4 gene product is an essential virulence protein requiring an intact nucleoside triphosphate-binding domain. J Bacteriol. 175:1993;1723-1734.
44. Kotob SI, Burns DL Essential role of the consensus nucleotide-binding site of PtlH in secretion of pertussis toxin from Bordetella pertussis. J Bacteriol. 179:1997;7577-7580.
45. Shirasu K, Koukolikova-Nicola Z, Hohn B, Kado CI An inner-membrane-associated virulence protein essential for T-DNA transfer from Agrobacterium tumefaciens to plants exhibits ATPase activity and similarities to conjugative transfer genes. Mol Microbiol. 11:1994;581-588.
46. Daugelavicius R, Bamford JKH, Grahn AM, Lanka E, Bamford DH The IncP plasmid-encoded cell envelope-associated DNA transfer complex increases cell permeability. J Bacteriol. 179:1997;5195-5202.
47. Christie PJ Agrobacterium tumefaciens T-complex transport apparatus: a paradigm for a new family of multifunctional tranporters in eubacteria. J Bacteriol. 179:1997;3085-3094.
48. Locht C, Keith JM Pertussis toxin gene: nucleotide sequence and genetic organization. Science. 232:1986;1258-1264.
49. Nicosia A, Perugini M, Franzini C, Casagli MC, Borri MG, Antoni G, Almoni M, Neri P, Ratti G, Rappuoli R Cloning and sequencing of the pertussis toxin genes: operon structure and gene duplication. Proc Natl Acad Sci USA. 83:1986;4631-4635.
50. Stein PE, Boodhoo A, Armstrong GD, Cockle SA, Klein MH, Read RJ The crystal structure of pertussis toxin. Structure. 2:1994;45-57.
51. Pizza M, Bugnoli M, Manetti R, Covacci A, Rappuoli R The subunit S1 is important for pertussis toxin secretion. J Biol Chem. 265:1990;17759-17763.
52. Winans SC, Burns DL, Christie PJ Adaptation of a conjugal transfer system for the export of pathogenic macromolecules. Trends Microbiol. 4:1996;64-68.
53. Burns DL, Manclark CR Adenine nucleotides promote dissociation of pertussis toxin subunits. J Biol Chem. 261:1986;4324-4327.