Type IV secretion systems: Versatility and diversity in function

Cellular Microbiology

Volumn 12, Issue 9, 2010, Pages 1203-1212

  Wallden, Karin ^a   Rivera Calzada, Angel ^a   Waksman, Gabriel ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE;

ADAPTATION; ANTIBIOTIC RESISTANCE; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM; COMPLEX FORMATION; CONFORMATION; CYTOPLASM; DNA PROTEIN COMPLEX; GENE TRANSFER; HOST CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; TYPE IV SECRETION SYSTEM;

BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; BIOLOGICAL TRANSPORT; CONJUGATION, GENETIC; DNA, BACTERIAL; GRAM-NEGATIVE BACTERIA; GRAM-POSITIVE BACTERIA; HUMANS; VIRULENCE FACTORS;

NEGIBACTERIA;

EID: 77957116092     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2010.01499.x     Document Type: Review

References (63)

1. Abajy MY, Kopec J, Schiwon K, Burzynski M, Doring M, Bohn C, Grohmann E. A type IV-secretion-like system is required for conjugative DNA transport of broad-host-range plasmid pIP501 in gram-positive bacteria. J Bacteriol 2007, 189:2487-2496.
2. Alvarez-Martinez CE, Christie PJ. Biological diversity of prokaryotic type IV secretion systems. Microbiol Mol Biol Rev 2009, 73:775-808.
3. Aly KA, Baron C. The VirB5 protein localizes to the T-pilus tips in Agrobacterium tumefaciens. Microbiology 2007, 153:3766-3775.
4. Andrzejewska J, Lee SK, Olbermann P, Lotzing N, Katzowitsch E, Linz B. Characterization of the pilin ortholog of the Helicobacter pylori type IV cag pathogenicity apparatus, a surface-associated protein expressed during infection. J Bacteriol 2006, 188:5865-5877.
5. Arechaga I, Pena A, Zunzunegui S, del Carmen Fernandez-Alonso M, Rivas G, de la Cruz F. ATPase activity and oligomeric state of TrwK, the VirB4 homologue of the plasmid R388 type IV secretion system. J Bacteriol 2008, 190:5472-5479.
6. Atmakuri K, Ding Z, Christie PJ. VirE2, a type IV secretion substrate, interacts with the VirD4 transfer protein at cell poles of Agrobacterium tumefaciens. Mol Microbiol 2003, 49:1699-1713.
7. Atmakuri K, Cascales E, Christie PJ. Energetic components VirD4, VirB11 and VirB4 mediate early DNA transfer reactions required for bacterial type IV secretion. Mol Microbiol 2004, 54:1199-1211.
8. Babic A, Lindner AB, Vulic M, Stewart EJ, Radman M. Direct visualization of horizontal gene transfer. Science 2008, 319:1533-1536.
9. Backert S, Meyer TF. Type IV secretion systems and their effectors in bacterial pathogenesis. Curr Opin Microbiol 2006, 9:207-217.
10. Backert S, Selbach M. Role of type IV secretion in Helicobacter pylori pathogenesis. Cell Microbiol 2008, 10:1573-1581.
11. Backert S, Fronzes R, Waksman G. VirB2 and VirB5 proteins: specialized adhesins in bacterial type-IV secretion systems? Trends Microbiol 2008, 16:409-413.
12. Bailey S, Ward D, Middleton R, Grossmann JG, Zambryski PC. Agrobacterium tumefaciens VirB8 structure reveals potential protein-protein interaction sites. Proc Natl Acad Sci USA 2006, 103:2582-2587.
13. 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 1997, 179:1203-1210.
14. Bradley DE. Morphological and serological relationships of conjugative pili. Plasmid 1980, 4:155-169.
15. Burns DL. Type IV transporters of pathogenic bacteria. Curr Opin Microbiol 2003, 6:29-34.
16. Cascales E, Christie PJ. Definition of a bacterial type IV secretion pathway for a DNA substrate. Science 2004, 304:1170-1173.
17. Chandran V, Fronzes R, Duquerroy S, Cronin N, Navaza J, Waksman G. Structure of the outer membrane complex of a type IV secretion system. Nature 2009, 462:1011-1015.
18. Christie PJ, Atmakuri K, Krishnamoorthy V, Jakubowski S, Cascales E. Biogenesis, architecture, and function of bacterial type IV secretion systems. Annu Rev Microbiol 2005, 59:451-485.
19. Craig-Mylius KA, Weiss AA. Mutants in the ptlA-H genes of Bordetella pertussis are deficient for pertussis toxin secretion. FEMS Microbiol Lett 1999, 179:479-484.
20. Dang TA, Zhou XR, Graf B, Christie PJ. Dimerization of the Agrobacterium tumefaciens VirB4 ATPase and the effect of ATP-binding cassette mutations on the assembly and function of the T-DNA transporter. Mol Microbiol 1999, 32:1239-1253.
21. Durand E, Oomen C, Waksman G. Biochemical dissection of the ATPase TraB, the VirB4 homologue of the Escherichia coli pKM101 conjugation machinery. J Bacteriol 2010, 192:2315-2323.
22. Eisenbrandt R, Kalkum M, Lai EM, Lurz R, Kado CI, Lanka E. Conjugative pili of IncP plasmids, and the Ti plasmid T pilus are composed of cyclic subunits. J Biol Chem 1999, 274:22548-22555.
23. Ensminger AW, Isberg RR. Legionella pneumophila Dot/Icm translocated substrates: a sum of parts. Curr Opin Microbiol 2009, 12:67-73.
24. Fronzes R, Christie PJ, Waksman G. The structural biology of type IV secretion systems. Nat Rev Microbiol 2009a, 7:703-714.
25. Fronzes R, Schafer E, Wang L, Saibil HR, Orlova EV, Waksman G. Structure of a type IV secretion system core complex. Science 2009b, 323:266-268.
26. Gomis-Ruth FX, Moncalian G, Perez-Luque R, Gonzalez A, Cabezon E, Cruz F, Coll M. The bacterial conjugation protein TrwB resembles ring helicases and F1-ATPase. Nature 2001, 409:637-641.
27. Grohmann E, Muth G, Espinosa M. Conjugative plasmid transfer in gram-positive bacteria. Microbiol Mol Biol Rev 2003, 67:277-301.
28. Hare S, Bayliss R, Baron C, Waksman G. A large domain swap in the VirB11 ATPase of Brucella suis leaves the hexameric assembly intact. J Mol Biol 2006, 360:56-66.
29. Hormaeche I, Alkorta I, Moro F, Valpuesta JM, Goni FM, De La Cruz F. Purification and properties of TrwB, a hexameric, ATP-binding integral membrane protein essential for R388 plasmid conjugation. J Biol Chem 2002, 277:46456-46462.
30. Ippen-Ihler KA, Minkley EG. The conjugation system of F, the fertility factor of Escherichia coli. Annu Rev Genet 1986, 20:593-624.
31. Jakubowski SJ, Kerr JE, Garza I, Krishnamoorthy V, Bayliss R, Waksman G, Christie PJ. Agrobacterium VirB10 domain requirements for type IV secretion and T pilus biogenesis. Mol Microbiol 2009, 71:779-794.
32. Juhas M, Crook DW, Hood DW. Type IV secretion systems: tools of bacterial horizontal gene transfer and virulence. Cell Microbiol 2008, 10:2377-2386.
33. Krause S, Barcena M, Pansegrau W, Lurz R, Carazo JM, Lanka E. Sequence-related protein export NTPases encoded by the conjugative transfer region of RP4 and by the cag pathogenicity island of Helicobacter pylori share similar hexameric ring structures. Proc Natl Acad Sci USA 2000a, 97:3067-3072.
34. Krause S, Pansegrau W, Lurz R, de la Cruz F, Lanka E. Enzymology of type IV macromolecule secretion systems: the conjugative transfer regions of plasmids RP4 and R388 and the cag pathogenicity island of Helicobacter pylori encode structurally and functionally related nucleoside triphosphate hydrolases. J Bacteriol 2000b, 182:2761-2770.
35. Kurenbach B, Bohn C, Prabhu J, Abudukerim M, Szewzyk U, Grohmann E. Intergeneric transfer of the Enterococcus faecalis plasmid pIP501 to Escherichia coli and Streptomyces lividans and sequence analysis of its tra region. Plasmid 2003, 50:86-93.
36. Kwok T, Zabler D, Urman S, Rohde M, Hartig R, Wessler S. Helicobacter exploits integrin for type IV secretion and kinase activation. Nature 2007, 449:862-866.
37. Lawley TD, Klimke WA, Gubbins MJ, Frost LS. F factor conjugation is a true type IV secretion system. FEMS Microbiol Lett 2003, 224:1-15.
38. Llosa M, Zupan J, Baron C, Zambryski P. The N- and C-terminal portions of the Agrobacterium VirB1 protein independently enhance tumorigenesis. J Bacteriol 2000, 182:3437-3445.
39. Moncalian G, Cabezon E, Alkorta I, Valle M, Moro F, Valpuesta JM. Characterization of ATP and DNA binding activities of TrwB, the coupling protein essential in plasmid R388 conjugation. J Biol Chem 1999, 274:36117-36124.
40. Mossey P, Hudacek A, Das A. Agrobacterium tumefaciens type IV secretion protein VirB3 is an inner membrane protein and requires VirB4, VirB7 and VirB8 for stabilization. J Bacteriol 2010, 192:2830-2838.
41. Nicosia A, Perugini M, Franzini C, Casagli MC, Borri MG, Antoni G. Cloning and sequencing of the pertussis toxin genes: operon structure and gene duplication. Proc Natl Acad Sci USA 1986, 83:4631-4635.
42. Ninio S, Roy CR. Effector proteins translocated by Legionella pneumophila: strength in numbers. Trends Microbiol 2007, 15:372-380.
43. Otter JA, French GL. Molecular epidemiology of community-associated meticillin-resistant Staphylococcus aureus in Europe. Lancet Infect Dis 2010, 10:227-239.
44. Rabel C, Grahn AM, Lurz R, Lanka E. The VirB4 family of proposed traffic nucleoside triphosphatases: common motifs in plasmid RP4 TrbE are essential for conjugation and phage adsorption. J Bacteriol 2003, 185:1045-1058.
45. Rambow-Larsen AA, Weiss AA. The PtlE protein of Bordetella pertussis has peptidoglycanase activity required for Ptl-mediated pertussis toxin secretion. J Bacteriol 2002, 184:2863-2869.
46. Rashkova S, Spudich GM, Christie PJ. Characterization of membrane and protein interaction determinants of the Agrobacterium tumefaciens VirB11 ATPase. J Bacteriol 1997, 179:583-591.
47. Rego AT, Chandran V, Waksman G. Two-step and one-step secretion mechanisms in Gram-negative bacteria: contrasting the type IV secretion system and the chaperone-usher pathway of pilus biogenesis. Biochem J 2010, 425:475-488.
48. Rivas S, Bolland S, Cabezon E, Goni FM, de la Cruz F. TrwD, a protein encoded by the IncW plasmid R388, displays an ATP hydrolase activity essential for bacterial conjugation. J Biol Chem 1997, 272:25583-25590.
49. Rohde M, Puls J, Buhrdorf R, Fischer W, Haas R. A novel sheathed surface organelle of the Helicobacter pylori cag type IV secretion system. Mol Microbiol 2003, 49:219-234.
50. Savvides SN, Yeo HJ, Beck MR, Blaesing F, Lurz R, Lanka E. VirB11 ATPases are dynamic hexameric assemblies: new insights into bacterial type IV secretion. EMBO J 2003, 22:1969-1980.
51. Schroder G, Krause S, Zechner EL, Traxler B, Yeo HJ, Lurz R. TraG-like proteins of DNA transfer systems and of the Helicobacter pylori type IV secretion system: inner membrane gate for exported substrates? J Bacteriol 2002, 184:2767-2779.
52. Sexton JA, Yeo HJ, Vogel JP. Genetic analysis of the Legionella pneumophila DotB ATPase reveals a role in type IV secretion system protein export. Mol Microbiol 2005, 57:70-84.
53. Shu AC, Wu CC, Chen YY, Peng HL, Chang HY, Yew TR. Evidence of DNA transfer through F-pilus channels during Escherichia coli conjugation. Langmuir 2008, 24:6796-6802.
54. Stingl K, Muller S, Scheidgen-Kleyboldt G, Clausen M, Maier B. Composite system mediates two-step DNA uptake into Helicobacter pylori. Proc Natl Acad Sci USA 2010, 107:1184-1189.
55. Tanaka J, Suzuki T, Mimuro H, Sasakawa C. Structural definition on the surface of Helicobacter pylori type IV secretion apparatus. Cell Microbiol 2003, 5:395-404.
56. Terradot L, Bayliss R, Oomen C, Leonard GA, Baron C, Waksman G. Structures of two core subunits of the bacterial type IV secretion system, VirB8 from Brucella suis and ComB10 from Helicobacter pylori. Proc Natl Acad Sci USA 2005, 102:4596-4601.
57. Verma A, Burns DL. Requirements for assembly of PtlH with the pertussis toxin transporter apparatus of Bordetella pertussis. Infect Immun 2007, 75:2297-2306.
58. Vincent CD, Friedman JR, Jeong KC, Buford EC, Miller JL, Vogel JP. Identification of the core transmembrane complex of the Legionella Dot/Icm type IV secretion system. Mol Microbiol 2006, 62:1278-1291.
59. 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.
60. Yeo HJ, Savvides SN, Herr AB, Lanka E, Waksman G. Crystal structure of the hexameric traffic ATPase of the Helicobacter pylori type IV secretion system. Mol Cell 2000, 6:1461-1472.
61. Yeo HJ, Yuan Q, Beck MR, Baron C, Waksman G. Structural and functional characterization of the VirB5 protein from the type IV secretion system encoded by the conjugative plasmid pKM101. Proc Natl Acad Sci USA 2003, 100:15947-15952.
62. Yuan Q, Carle A, Gao C, Sivanesan D, Aly KA, Hoppner C. Identification of the VirB4-VirB8-VirB5-VirB2 pilus assembly sequence of type IV secretion systems. J Biol Chem 2005, 280:26349-26359.
63. Zupan J, Hackworth CA, Aguilar J, Ward D, Zambryski P. VirB1* promotes T-pilus formation in the vir-Type IV secretion system of Agrobacterium tumefaciens. J Bacteriol 2007, 189:6551-6563.