1932

Abstract

Type IV secretion systems (T4SSs) are large multisubunit translocons, found in both gram-negative and gram-positive bacteria and in some archaea. These systems transport a diverse array of substrates from DNA and protein–DNA complexes to proteins, and play fundamental roles in both bacterial pathogenesis and bacterial adaptation to the cellular milieu in which bacteria live. This review describes the various biochemical and structural advances made toward understanding the biogenesis, architecture, and function of T4SSs.

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2015-06-02
2024-06-13
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Literature Cited

  1. Terradot L, Waksman G. 1.  2011. Architecture of the Helicobacter pylori Cag-type IV secretion system. FEBS J. 278:1213–22 [Google Scholar]
  2. McCullen CA, Binns AN. 2.  2006. Agrobacterium tumefaciens and plant cell interactions and activities required for interkingdom macromolecular transfer. Annu. Rev. Cell Dev. Biol. 22:101–27 [Google Scholar]
  3. Hofreuter D, Odenbreit S, Henke G, Haas R. 3.  1998. Natural competence for DNA transformation in Helicobacter pylori: identification and genetic characterization of the comB locus. Mol. Microbiol. 28:1027–38 [Google Scholar]
  4. Hamilton HL, Dillard JP. 4.  2006. Natural transformation of Neisseria gonorrhoeae: from DNA donation to homologous recombination. Mol. Microbiol. 59:376–85 [Google Scholar]
  5. Juhas M, Crook DW, Dimopoulou ID, Lunter G, Harding RM. 5.  et al. 2007. Novel type IV secretion system involved in propagation of genomic islands. J. Bacteriol. 189:761–71 [Google Scholar]
  6. Ninio S, Roy CR. 6.  2007. Effector proteins translocated by Legionella pneumophila: strength in numbers. Trends Microbiol. 15:372–80 [Google Scholar]
  7. Guglielmini J, Neron B, Abby SS, Garcillan-Barcia MP, de la Cruz F, Rocha EP. 7.  2014. Key components of the eight classes of type IV secretion systems involved in bacterial conjugation or protein secretion. Nucleic Acids Res. 42:5715–27 [Google Scholar]
  8. Hofreuter D, Odenbreit S, Haas R. 8.  2001. Natural transformation competence in Helicobacter pylori is mediated by the basic components of a type IV secretion system. Mol. Microbiol. 41:379–91 [Google Scholar]
  9. Hamilton HL, Dominguez NM, Schwartz KJ, Hackett KT, Dillard JP. 9.  2005. Neisseria gonorrhoeae secretes chromosomal DNA via a novel type IV secretion system. Mol. Microbiol. 55:1704–21 [Google Scholar]
  10. Salgado-Pabon W, Jain S, Turner N, van der Does C, Dillard JP. 10.  2007. A novel relaxase homologue is involved in chromosomal DNA processing for type IV secretion in Neisseria gonorrhoeae. Mol. Microbiol. 66:930–47 [Google Scholar]
  11. Novick RP. 11.  1987. Plasmid incompatibility. Microbiol. Rev. 51:381–95 [Google Scholar]
  12. Lawley TD, Klimke WA, Gubbins MJ, Frost LS. 12.  2003. F factor conjugation is a true type IV secretion system. FEMS Microbiol. Lett. 224:1–15 [Google Scholar]
  13. Komano T, Yoshida T, Narahara K, Furuya N. 13.  2000. The transfer region of IncI1 plasmid R64: similarities between R64 tra and Legionella icm/dot genes. Mol. Microbiol. 35:1348–59 [Google Scholar]
  14. Nagai H, Kubori T. 14.  2011. Type IVB secretion systems of Legionella and other gram-negative bacteria. Front. Microbiol. 2:136 [Google Scholar]
  15. Pattis I, Weiss E, Laugks R, Haas R, Fischer W. 15.  2007. The Helicobacter pylori CagF protein is a type IV secretion chaperone-like molecule that binds close to the C-terminal secretion signal of the CagA effector protein. Microbiology 153:2896–909 [Google Scholar]
  16. Dym O, Albeck S, Unger T, Jacobovitch J, Branzburg A. 16.  et al. 2008. Crystal structure of the Agrobacterium virulence complex VirE1–VirE2 reveals a flexible protein that can accommodate different partners. PNAS 105:11170–75 [Google Scholar]
  17. Sutherland MC, Nguyen TL, Tseng V, Vogel JP. 17.  2012. The Legionella IcmSW complex directly interacts with DotL to mediate translocation of adaptor-dependent substrates. PLOS Pathog. 8:e1002910 [Google Scholar]
  18. Sakalis PA, van Heusden GP, Hooykaas PJ. 18.  2014. Visualization of VirE2 protein translocation by the Agrobacterium type IV secretion system into host cells. MicrobiologyOpen 3:104–17 [Google Scholar]
  19. Alvarez-Martinez CE, Christie PJ. 19.  2009. Biological diversity of prokaryotic type IV secretion systems. Microbiol. Mol. Biol. Rev. 73:775–808 [Google Scholar]
  20. Christie PJ, Atmakuri K, Krishnamoorthy V, Jakubowski S, Cascales E. 20.  2005. Biogenesis, architecture, and function of bacterial type IV secretion systems. Annu. Rev. Microbiol. 59:451–85 [Google Scholar]
  21. Bhatty M, Laverde Gomez JA, Christie PJ. 21.  2013. The expanding bacterial type IV secretion lexicon. Res. Microbiol. 164:620–39 [Google Scholar]
  22. Low HH, Gubellini F, Rivera-Calzada A, Braun N, Connery S. 22.  et al. 2014. Structure of a type IV secretion system. Nature 508:550–53 [Google Scholar]
  23. Berger BR, Christie PJ. 23.  1994. Genetic complementation analysis of the Agrobacterium tumefaciens virB operon: virB2 through virB11 are essential virulence genes. J. Bacteriol. 176:3646–60 [Google Scholar]
  24. Zupan J, Hackworth CA, Aguilar J, Ward D, Zambryski P. 24.  2007. VirB1* promotes T-pilus formation in the vir type IV secretion system of Agrobacterium tumefaciens. J. Bacteriol. 189:6551–63 [Google Scholar]
  25. Berry TM, Christie PJ. 25.  2011. Caught in the act: the dialogue between bacteriophage R17 and the type IV secretion machine of plasmid R1. Mol. Microbiol. 82:1039–43 [Google Scholar]
  26. Lai EM, Chesnokova O, Banta LM, Kado CI. 26.  2000. Genetic and environmental factors affecting T-pilin export and T-pilus biogenesis in relation to flagellation of Agrobacterium tumefaciens. J. Bacteriol. 182:3705–16 [Google Scholar]
  27. Seubert A, Falch C, Birtles RJ, Schulein R, Dehio C. 27.  2003. Characterization of the cryptic plasmid pBGR1 from Bartonella grahamii and construction of a versatile Escherichia coli–Bartonella spp. shuttle cloning vector. Plasmid 49:44–52 [Google Scholar]
  28. Moncalian G, Cabezon E, Alkorta I, Valle M, Moro F. 28.  et al. 1999. Characterization of ATP and DNA binding activities of TrwB, the coupling protein essential in plasmid R388 conjugation. J. Biol. Chem. 274:36117–24 [Google Scholar]
  29. Tato I, Zunzunegui S, de la Cruz F, Cabezon E. 29.  2005. TrwB, the coupling protein involved in DNA transport during bacterial conjugation, is a DNA-dependent ATPase. PNAS 102:8156–61 [Google Scholar]
  30. Hormaeche I, Iloro I, Arrondo JL, Goni FM, de la Cruz F, Alkorta I. 30.  2004. Role of the transmembrane domain in the stability of TrwB, an integral protein involved in bacterial conjugation. J. Biol. Chem. 279:10955–61 [Google Scholar]
  31. Pena A, Matilla I, Martin-Benito J, Valpuesta JM, Carrascosa JL. 31.  et al. 2012. The hexameric structure of a conjugative VirB4 protein ATPase provides new insights for a functional and phylogenetic relationship with DNA translocases. J. Biol. Chem. 287:39925–32 [Google Scholar]
  32. Tato I, Matilla I, Arechaga I, Zunzunegui S, de la Cruz F, Cabezon E. 32.  2007. The ATPase activity of the DNA transporter TrwB is modulated by protein TrwA: implications for a common assembly mechanism of DNA translocating motors. J. Biol. Chem. 282:25569–76 [Google Scholar]
  33. Beranek A, Zettl M, Lorenzoni K, Schauer A, Manhart M, Koraimann G. 33.  2004. Thirty-eight C-terminal amino acids of the coupling protein TraD of the F-like conjugative resistance plasmid R1 are required and sufficient to confer binding to the substrate selector protein TraM. J. Bacteriol. 186:6999–7006 [Google Scholar]
  34. Matilla I, Alfonso C, Rivas G, Bolt EL, de la Cruz F, Cabezon E. 34.  2010. The conjugative DNA translocase TrwB is a structure-specific DNA-binding protein. J. Biol. Chem. 285:17537–44 [Google Scholar]
  35. de Paz HD, Sangari FJ, Bolland S, Garcia-Lobo JM, Dehio C. 35.  et al. 2005. Functional interactions between type IV secretion systems involved in DNA transfer and virulence. Microbiology 151:3505–16 [Google Scholar]
  36. de Paz HD, Larrea D, Zunzunegui S, Dehio C, de la Cruz F, Llosa M. 36.  2010. Functional dissection of the conjugative coupling protein TrwB. J. Bacteriol. 192:2655–69 [Google Scholar]
  37. Atmakuri K, Cascales E, Christie PJ. 37.  2004. Energetic components VirD4, VirB11 and VirB4 mediate early DNA transfer reactions required for bacterial type IV secretion. Mol. Microbiol. 54:1199–211 [Google Scholar]
  38. Ripoll-Rozada J, Zunzunegui S, de la Cruz F, Arechaga I, Cabezon E. 38.  2013. Functional interactions of VirB11 traffic ATPases with VirB4 and VirD4 molecular motors in type IV secretion systems. J. Bacteriol. 195:4195–201 [Google Scholar]
  39. Shirasu K, Koukolikova-Nicola Z, Hohn B, Kado CI. 39.  1994. 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. 11:581–88 [Google Scholar]
  40. Dang TA, Christie PJ. 40.  1997. The VirB4 ATPase of Agrobacterium tumefaciens is a cytoplasmic membrane protein exposed at the periplasmic surface. J. Bacteriol. 179:453–62 [Google Scholar]
  41. Rabel C, Grahn AM, Lurz R, Lanka E. 41.  2003. The VirB4 family of proposed traffic nucleoside triphosphatases: Common motifs in plasmid RP4 TrbE are essential for conjugation and phage adsorption. J. Bacteriol. 185:1045–58 [Google Scholar]
  42. Fullner KJ, Stephens KM, Nester EW. 42.  1994. An essential virulence protein of Agrobacterium tumefaciens, VirB4, requires an intact mononucleotide binding domain to function in transfer of T-DNA. Mol. Gen. Genet. 245:704–15 [Google Scholar]
  43. Berger BR, Christie PJ. 43.  1993. The Agrobacterium tumefaciens virB4 gene product is an essential virulence protein requiring an intact nucleoside triphosphate-binding domain. J. Bacteriol. 175:1723–34 [Google Scholar]
  44. Watarai M, Makino S, Shirahata T. 44.  2002. An essential virulence protein of Brucella abortus, VirB4, requires an intact nucleoside-triphosphate-binding domain. Microbiology 148:1439–46 [Google Scholar]
  45. Arechaga I, Pena A, Zunzunegui S, del Carmen Fernandez–Alonso M, Rivas G, de la Cruz F. 45.  2008. ATPase activity and oligomeric state of TrwK, the VirB4 homologue of the plasmid R388 type IV secretion system. J. Bacteriol. 190:5472–79 [Google Scholar]
  46. Durand E, Oomen C, Waksman G. 46.  2010. Biochemical dissection of the ATPase TraB, the VirB4 homologue of the Escherichia coli pKM101 conjugation machinery. J. Bacteriol. 192:2315–23 [Google Scholar]
  47. Pena A, Ripoll-Rozada J, Zunzunegui S, Cabezon E, de la Cruz F, Arechaga I. 47.  2011. Autoinhibitory regulation of TrwK, an essential VirB4 ATPase in type IV secretion systems. J. Biol. Chem. 286:17376–82 [Google Scholar]
  48. Li F, Alvarez-Martinez C, Chen Y, Choi KJ, Yeo HJ, Christie PJ. 48.  2012. Enterococcus faecalis PrgJ, a VirB4-like ATPase, mediates pCF10 conjugative transfer through substrate binding. J. Bacteriol. 194:4041–51 [Google Scholar]
  49. Schandel KA, Muller MM, Webster RE. 49.  1992. Localization of TraC, a protein involved in assembly of the F conjugative pilus. J. Bacteriol. 174:3800–6 [Google Scholar]
  50. Draper O, Middleton R, Doucleff M, Zambryski PC. 50.  2006. Topology of the VirB4 C terminus in the Agrobacterium tumefaciens VirB/D4 type IV secretion system. J. Biol. Chem. 281:37628–35 [Google Scholar]
  51. Dang TA, Zhou XR, Graf B, Christie PJ. 51.  1999. 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. 32:1239–53 [Google Scholar]
  52. Planet PJ, Kachlany SC, DeSalle R, Figurski DH. 52.  2001. Phylogeny of genes for secretion NTPases: identification of the widespread tadA subfamily and development of a diagnostic key for gene classification. PNAS 98:2503–8 [Google Scholar]
  53. Rivas S, Bolland S, Cabezon E, Goni FM, de la Cruz F. 53.  1997. TrwD, a protein encoded by the IncW plasmid R388, displays an ATP hydrolase activity essential for bacterial conjugation. J. Biol. Chem. 272:25583–90 [Google Scholar]
  54. Rashkova S, Spudich GM, Christie PJ. 54.  1997. Characterization of membrane and protein interaction determinants of the Agrobacterium tumefaciens VirB11 ATPase. J. Bacteriol. 179:583–91 [Google Scholar]
  55. Krause S, Pansegrau W, Lurz R, de la Cruz F, Lanka E. 55.  2000. 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. 182:2761–70 [Google Scholar]
  56. Christie PJ, Ward JE Jr., Gordon MP, Nester EW. 56.  1989. A gene required for transfer of T-DNA to plants encodes an ATPase with autophosphorylating activity. PNAS 86:9677–81 [Google Scholar]
  57. Ripoll-Rozada J, Pena A, Rivas S, Moro F, de la Cruz F. 57.  et al. 2012. Regulation of the type IV secretion ATPase TrwD by magnesium: implications for catalytic mechanism of the secretion ATPase superfamily. J. Biol. Chem. 287:17408–14 [Google Scholar]
  58. Jones AL, Shirasu K, Kado CI. 58.  1994. The product of the virB4 gene of Agrobacterium tumefaciens promotes accumulation of VirB3 protein. J. Bacteriol. 176:5255–61 [Google Scholar]
  59. Beijersbergen A, Smith SJ, Hooykaas PJ. 59.  1994. Localization and topology of VirB proteins of Agrobacterium tumefaciens. Plasmid 32:212–18 [Google Scholar]
  60. Shirasu K, Kado CI. 60.  1993. Membrane location of the Ti plasmid VirB proteins involved in the biosynthesis of a pilin-like conjugative structure on Agrobacterium tumefaciens. FEMS Microbiol. Lett. 111:287–94 [Google Scholar]
  61. Mossey P, Hudacek A, Das A. 61.  2010. Agrobacterium tumefaciens type IV secretion protein VirB3 is an inner membrane protein and requires VirB4, VirB7, and VirB8 for stabilization. J. Bacteriol. 192:2830–38 [Google Scholar]
  62. Batchelor RA, Pearson BM, Friis LM, Guerry P, Wells JM. 62.  2004. Nucleotide sequences and comparison of two large conjugative plasmids from different Campylobacter species. Microbiology 150:3507–17 [Google Scholar]
  63. Hapfelmeier S, Domke N, Zambryski PC, Baron C. 63.  2000. VirB6 is required for stabilization of VirB5 and VirB3 and formation of VirB7 homodimers in Agrobacterium tumefaciens. J. Bacteriol. 182:4505–11 [Google Scholar]
  64. Shamaei-Tousi A, Cahill R, Frankel G. 64.  2004. Interaction between protein subunits of the type IV secretion system of Bartonella henselae. J. Bacteriol. 186:4796–801 [Google Scholar]
  65. Jakubowski SJ, Krishnamoorthy V, Cascales E, Christie PJ. 65.  2004. Agrobacterium tumefaciens VirB6 domains direct the ordered export of a DNA substrate through a type IV secretion system. J. Mol. Biol. 341:961–77 [Google Scholar]
  66. Karnholz A, Hoefler C, Odenbreit S, Fischer W, Hofreuter D, Haas R. 66.  2006. Functional and topological characterization of novel components of the comB DNA transformation competence system in Helicobacter pylori. J. Bacteriol. 188:882–93 [Google Scholar]
  67. Jakubowski SJ, Krishnamoorthy V, Christie PJ. 67.  2003. Agrobacterium tumefaciens VirB6 protein participates in formation of VirB7 and VirB9 complexes required for type IV secretion. J. Bacteriol. 185:2867–78 [Google Scholar]
  68. Kumar RB, Xie YH, Das A. 68.  2000. Subcellular localization of the Agrobacterium tumefaciens T-DNA transport pore proteins: VirB8 is essential for the assembly of the transport pore. Mol. Microbiol. 36:608–17 [Google Scholar]
  69. Das A, Xie YH. 69.  1998. Construction of transposon Tn3phoA: its application in defining the membrane topology of the Agrobacterium tumefaciens DNA transfer proteins. Mol. Microbiol. 27:405–14 [Google Scholar]
  70. Paschos A, Patey G, Sivanesan D, Gao C, Bayliss R. 70.  et al. 2006. Dimerization and interactions of Brucella suis VirB8 with VirB4 and VirB10 are required for its biological activity. PNAS 103:7252–57 [Google Scholar]
  71. Kumar RB, Das A. 71.  2001. Functional analysis of the Agrobacterium tumefaciens T-DNA transport pore protein VirB8. J. Bacteriol. 183:3636–41 [Google Scholar]
  72. Krall L, Wiedemann U, Unsin G, Weiss S, Domke N, Baron C. 72.  2002. Detergent extraction identifies different VirB protein subassemblies of the type IV secretion machinery in the membranes of Agrobacterium tumefaciens. PNAS 99:11405–10 [Google Scholar]
  73. Ward DV, Draper O, Zupan JR, Zambryski PC. 73.  2002. Peptide linkage mapping of the Agrobacterium tumefaciens vir-encoded type IV secretion system reveals protein subassemblies. PNAS 99:11493–500 [Google Scholar]
  74. Yuan Q, Carle A, Gao C, Sivanesan D, Aly KA. 74.  et al. 2005. Identification of the VirB4-VirB8-VirB5-VirB2 pilus assembly sequence of type IV secretion systems. J. Biol. Chem. 280:26349–59 [Google Scholar]
  75. Hoppner C, Carle A, Sivanesan D, Hoeppner S, Baron C. 75.  2005. The putative lytic transglycosylase VirB1 from Brucella suis interacts with the type IV secretion system core components VirB8, VirB9 and VirB11. Microbiology 151:3469–82 [Google Scholar]
  76. Das A, Xie YH. 76.  2000. The Agrobacterium T-DNA transport pore proteins VirB8, VirB9, and VirB10 interact with one another. J. Bacteriol. 182:758–63 [Google Scholar]
  77. Villamil Giraldo AM, Sivanesan D, Carle A, Paschos A, Smith MA. 77.  et al. 2012. Type IV secretion system core component VirB8 from Brucella binds to the globular domain of VirB5 and to a periplasmic domain of VirB6. Biochemistry 51:3881–90 [Google Scholar]
  78. Bourg G, Sube R, O'Callaghan D, Patey G. 78.  2009. Interactions between Brucella suis VirB8 and its homolog TraJ from the plasmid pSB102 underline the dynamic nature of type IV secretion systems. J. Bacteriol. 191:2985–92 [Google Scholar]
  79. Patey G, Qi Z, Bourg G, Baron C, O'Callaghan D. 79.  2006. Swapping of periplasmic domains between Brucella suis VirB8 and a pSB102 VirB8 homologue allows heterologous complementation. Infect. Immun. 74:4945–49 [Google Scholar]
  80. Sivanesan D, Baron C. 80.  2011. The dimer interface of Agrobacterium tumefaciens VirB8 is important for type IV secretion system function, stability, and association of VirB2 with the core complex. J. Bacteriol. 193:2097–106 [Google Scholar]
  81. Tsai YL, Chiang YR, Narberhaus F, Baron C, Lai EM. 81.  2010. The small heat-shock protein HspL is a VirB8 chaperone promoting type IV secretion-mediated DNA transfer. J. Biol. Chem. 285:19757–66 [Google Scholar]
  82. Fronzes R, Schafer E, Wang L, Saibil HR, Orlova EV, Waksman G. 82.  2009. Structure of a type IV secretion system core complex. Science 323:266–68 [Google Scholar]
  83. Fernandez D, Dang TA, Spudich GM, Zhou XR, Berger BR, Christie PJ. 83.  1996. 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. 178:3156–67 [Google Scholar]
  84. Baron C, Thorstenson YR, Zambryski PC. 84.  1997. The lipoprotein VirB7 interacts with VirB9 in the membranes of Agrobacterium tumefaciens. J. Bacteriol. 179:1211–18 [Google Scholar]
  85. Spudich GM, Fernandez D, Zhou XR, Christie PJ. 85.  1996. Intermolecular disulfide bonds stabilize VirB7 homodimers and VirB7/VirB9 heterodimers during biogenesis of the Agrobacterium tumefaciens T-complex transport apparatus. PNAS 93:7512–17 [Google Scholar]
  86. Sagulenko V, Sagulenko E, Jakubowski S, Spudich E, Christie PJ. 86.  2001. VirB7 lipoprotein is exocellular and associates with the Agrobacterium tumefaciens T pilus. J. Bacteriol. 183:3642–51 [Google Scholar]
  87. Souza DP, Andrade MO, Alvarez-Martinez CE, Arantes GM, Farah CS, Salinas RK. 87.  2011. A component of the Xanthomonadaceae type IV secretion system combines a VirB7 motif with a N0 domain found in outer membrane transport proteins. PLOS Pathog. 7:e1002031 [Google Scholar]
  88. Beaupre CE, Bohne J, Dale EM, Binns AN. 88.  1997. Interactions between VirB9 and VirB10 membrane proteins involved in movement of DNA from Agrobacterium tumefaciens into plant cells. J. Bacteriol. 179:78–89 [Google Scholar]
  89. Jakubowski SJ, Cascales E, Krishnamoorthy V, Christie PJ. 89.  2005. Agrobacterium tumefaciens VirB9, an outer-membrane-associated component of a type IV secretion system, regulates substrate selection and T-pilus biogenesis. J. Bacteriol. 187:3486–95 [Google Scholar]
  90. Chandran V, Fronzes R, Duquerroy S, Cronin N, Navaza J, Waksman G. 90.  2009. Structure of the outer membrane complex of a type IV secretion system. Nature 462:1011–15 [Google Scholar]
  91. Jakubowski SJ, Kerr JE, Garza I, Krishnamoorthy V, Bayliss R. 91.  et al. 2009. Agrobacterium VirB10 domain requirements for type IV secretion and T pilus biogenesis. Mol. Microbiol. 71:779–94 [Google Scholar]
  92. Cascales E, Christie PJ. 92.  2004. Agrobacterium VirB10, an ATP energy sensor required for type IV secretion. PNAS 101:17228–33 [Google Scholar]
  93. Banta LM, Kerr JE, Cascales E, Giuliano ME, Bailey ME. 93.  et al. 2011. An Agrobacterium VirB10 mutation conferring a type IV secretion system gating defect. J. Bacteriol. 193:2566–74 [Google Scholar]
  94. Zahrl D, Wagner M, Bischof K, Bayer M, Zavecz B. 94.  et al. 2005. Peptidoglycan degradation by specialized lytic transglycosylases associated with type III and type IV secretion systems. Microbiology 151:3455–67 [Google Scholar]
  95. Koraimann G. 95.  2003. Lytic transglycosylases in macromolecular transport systems of gram-negative bacteria. Cell. Mol. Life Sci. 60:2371–88 [Google Scholar]
  96. Fullner KJ, Lara JC, Nester EW. 96.  1996. Pilus assembly by Agrobacterium T-DNA transfer genes. Science 273:1107–9 [Google Scholar]
  97. Rohde M, Puls J, Buhrdorf R, Fischer W, Haas R. 97.  2003. A novel sheathed surface organelle of the Helicobacter pylori cag type IV secretion system. Mol. Microbiol. 49:219–34 [Google Scholar]
  98. Baron C, Llosa M, Zhou S, Zambryski PC. 98.  1997. VirB1, a component of the T-complex transfer machinery of Agrobacterium tumefaciens, is processed to a C-terminal secreted product, VirB1. J. Bacteriol. 179:1203–10 [Google Scholar]
  99. Llosa M, Zupan J, Baron C, Zambryski P. 99.  2000. The N- and C-terminal portions of the Agrobacterium VirB1 protein independently enhance tumorigenesis. J. Bacteriol. 182:3437–45 [Google Scholar]
  100. Lai EM, Eisenbrandt R, Kalkum M, Lanka E, Kado CI. 100.  2002. Biogenesis of T pili in Agrobacterium tumefaciens requires precise VirB2 propilin cleavage and cyclization. J. Bacteriol. 184:327–30 [Google Scholar]
  101. Jones AL, Lai EM, Shirasu K, Kado CI. 101.  1996. VirB2 is a processed pilin-like protein encoded by the Agrobacterium tumefaciens Ti plasmid. J. Bacteriol. 178:5706–11 [Google Scholar]
  102. Kerr JE, Christie PJ. 102.  2010. Evidence for VirB4-mediated dislocation of membrane-integrated VirB2 pilin during biogenesis of the Agrobacterium VirB/VirD4 type IV secretion system. J. Bacteriol. 192:4923–34 [Google Scholar]
  103. Schmidt-Eisenlohr H, Domke N, Angerer C, Wanner G, Zambryski PC, Baron C. 103.  1999. Vir proteins stabilize VirB5 and mediate its association with the T pilus of Agrobacterium tumefaciens. J. Bacteriol. 181:7485–92 [Google Scholar]
  104. Aly KA, Baron C. 104.  2007. The VirB5 protein localizes to the T-pilus tips in Agrobacterium tumefaciens. Microbiology 153:3766–75 [Google Scholar]
  105. Rivera-Calzada A, Fronzes R, Savva CG, Chandran V, Lian PW. 105.  et al. 2013. Structure of a bacterial type IV secretion core complex at subnanometre resolution. EMBO J. 32:1195–204 [Google Scholar]
  106. Wallden K, Williams R, Yan J, Lian PW, Wang L. 106.  et al. 2012. Structure of the VirB4 ATPase, alone and bound to the core complex of a type IV secretion system. PNAS 109:11348–53 [Google Scholar]
  107. Wang YA, Yu X, Silverman PM, Harris RL, Egelman EH. 107.  2009. The structure of F-pili. J. Mol. Biol. 385:22–29 [Google Scholar]
  108. Gomis-Ruth FX, Coll M. 108.  2001. Structure of TrwB, a gatekeeper in bacterial conjugation. Int. J. Biochem. Cell Biol. 33:839–43 [Google Scholar]
  109. Gomis-Ruth FX, Moncalian G, de la Cruz F, Coll M. 109.  2002. Conjugative plasmid protein TrwB, an integral membrane type IV secretion system coupling protein. Detailed structural features and mapping of the active site cleft. J. Biol. Chem. 277:7556–66 [Google Scholar]
  110. Yeo HJ, Savvides SN, Herr AB, Lanka E, Waksman G. 110.  2000. Crystal structure of the hexameric traffic ATPase of the Helicobacter pylori type IV secretion system. Mol. Cell 6:1461–72 [Google Scholar]
  111. Savvides SN, Yeo HJ, Beck MR, Blaesing F, Lurz R. 111.  et al. 2003. VirB11 ATPases are dynamic hexameric assemblies: new insights into bacterial type IV secretion. EMBO J. 22:1969–80 [Google Scholar]
  112. Hare S, Bayliss R, Baron C, Waksman G. 112.  2006. A large domain swap in the VirB11 ATPase of Brucella suis leaves the hexameric assembly intact. J. Mol. Biol. 360:56–66 [Google Scholar]
  113. Terradot L, Bayliss R, Oomen C, Leonard GA, Baron C, Waksman G. 113.  2005. Structures of two core subunits of the bacterial type IV secretion system, VirB8 from Brucella suis and ComB10 from Helicobacter pylori. PNAS 102:4596–601 [Google Scholar]
  114. Bailey S, Ward D, Middleton R, Grossmann JG, Zambryski PC. 114.  2006. Agrobacterium tumefaciens VirB8 structure reveals potential protein–protein interaction sites. PNAS 103:2582–87 [Google Scholar]
  115. Bayliss R, Harris R, Coutte L, Monier A, Fronzes R. 115.  et al. 2007. NMR structure of a complex between the VirB9/VirB7 interaction domains of the pKM101 type IV secretion system. PNAS 104:1673–78 [Google Scholar]
  116. Yeo HJ, Yuan Q, Beck MR, Baron C, Waksman G. 116.  2003. Structural and functional characterization of the VirB5 protein from the type IV secretion system encoded by the conjugative plasmid pKM101. PNAS 100:15947–52 [Google Scholar]
  117. Dong C, Beis K, Nesper J, Brunkan-Lamontagne AL, Clarke BR. 117.  et al. 2006. Wza the translocon for E. coli capsular polysaccharides defines a new class of membrane protein. Nature 444:226–29 [Google Scholar]
  118. Middleton R, Sjolander K, Krishnamurthy N, Foley J, Zambryski P. 118.  2005. Predicted hexameric structure of the Agrobacterium VirB4 C terminus suggests VirB4 acts as a docking site during type IV secretion. PNAS 102:1685–90 [Google Scholar]
  119. Backert S, Clyne M, Tegtmeyer N. 119.  2011. Molecular mechanisms of gastric epithelial cell adhesion and injection of CagA by Helicobacter pylori. Cell Commun. Signal. 9:28 [Google Scholar]
  120. Cendron L, Zanotti G. 120.  2011. Structural and functional aspects of unique type IV secretory components in the Helicobacter pylori cag-pathogenicity island. FEBS J. 278:1223–31 [Google Scholar]
  121. Cendron L, Seydel A, Angelini A, Battistutta R, Zanotti G. 121.  2004. Crystal structure of CagZ, a protein from the Helicobacter pylori pathogenicity island that encodes for a type IV secretion system. J. Mol. Biol. 340:881–89 [Google Scholar]
  122. Cendron L, Tasca E, Seraglio T, Seydel A, Angelini A. 122.  et al. 2007. The crystal structure of CagS from the Helicobacter pylori pathogenicity island. Proteins 69:440–43 [Google Scholar]
  123. Cendron L, Couturier M, Angelini A, Barison N, Stein M, Zanotti G. 123.  2009. The Helicobacter pylori CagD (HP0545, Cag24) protein is essential for CagA translocation and maximal induction of interleukin-8 secretion. J. Mol. Biol. 386:204–17 [Google Scholar]
  124. Backert S, Fronzes R, Waksman G. 124.  2008. VirB2 and VirB5 proteins: specialized adhesins in bacterial type-IV secretion systems?. Trends Microbiol. 16:409–13 [Google Scholar]
  125. Nakano N, Kubori T, Kinoshita M, Imada K, Nagai H. 125.  2010. Crystal structure of Legionella DotD: insights into the relationship between type IVB and type II/III secretion systems. PLOS Pathog. 6:e1001129 [Google Scholar]
  126. Porter CJ, Bantwal R, Bannam TL, Rosado CJ, Pearce MC. 126.  et al. 2011. The conjugation protein TcpC from Clostridium perfringens is structurally related to the type IV secretion system protein VirB8 from gram-negative bacteria. Mol. Microbiol. 83:275–88 [Google Scholar]
  127. Judd PK, Kumar RB, Das A. 127.  2005. Spatial location and requirements for the assembly of the Agrobacterium tumefaciens type IV secretion apparatus. PNAS 102:11498–503 [Google Scholar]
  128. Aguilar J, Zupan J, Cameron TA, Zambryski PC. 128.  2010. Agrobacterium type IV secretion system and its substrates form helical arrays around the circumference of virulence-induced cells. PNAS 107:3758–63 [Google Scholar]
  129. Babic A, Lindner AB, Vulic M, Stewart EJ, Radman M. 129.  2008. Direct visualization of horizontal gene transfer. Science 319:1533–36 [Google Scholar]
  130. Mota LJ, Journet L, Sorg I, Agrain C, Cornelis GR. 130.  2005. Bacterial injectisomes: needle length does matter. Science 307:1278 [Google Scholar]
  131. Cascales E, Christie PJ. 131.  2004. Definition of a bacterial type IV secretion pathway for a DNA substrate. Science 304:1170–73 [Google Scholar]
  132. Shu AC, Wu CC, Chen YY, Peng HL, Chang HY, Yew TR. 132.  2008. Evidence of DNA transfer through F-pilus channels during Escherichia coli conjugation. Langmuir 24:6796–802 [Google Scholar]
  133. Kwok T, Zabler D, Urman S, Rohde M, Hartig R. 133.  et al. 2007. Helicobacter exploits integrin for type IV secretion and kinase activation. Nature 449:862–66 [Google Scholar]
  134. Radics J, Konigsmaier L, Marlovits TC. 134.  2014. Structure of a pathogenic type 3 secretion system in action. Nat. Struct. Mol. Biol. 21:82–87 [Google Scholar]
  135. Phan G, Remaut H, Wang T, Allen WJ, Pirker KF. 135.  et al. 2011. Crystal structure of the FimD usher bound to its cognate FimC–FimH substrate. Nature 474:49–53 [Google Scholar]
  136. Geibel S, Procko E, Hultgren SJ, Baker D, Waksman G. 136.  2013. Structural and energetic basis of folded-protein transport by the FimD usher. Nature 496:243–46 [Google Scholar]
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