Coupling Proteins in Type IV Secretion

Chapter
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 413)

Abstract

Type IV coupling proteins (T4CPs) are essential constituents of most type IV secretion systems (T4SSs), and probably the most intriguing component in terms of their evolutionary origin and functional role. Coupling proteins have coevolved with their cognate secretion system and translocated substrates. They are present in all conjugative systems, leading to the suggestion that they play a specific role in DNA transfer. However, they are also part of many T4SSs involved in bacterial virulence, where they are required for protein translocation, with no apparent involvement in DNA secretion. Their name reflects genetic and biochemical evidence of a connecting role between the substrate and the T4SS, thus probably playing a major role in substrate recruitment. Increasing evidence supports also a role in signal transmission leading to activation of secretion. Most studies have addressed conjugative coupling proteins of the VirD4-like protein family. Their conserved features include a nucleotide-binding domain, essential for substrate translocation, a C-terminal domain involved in substrate interactions, and a transmembrane domain anchoring them to the inner membrane, which is an important regulator of protein function. Purified soluble deletion mutants display ATP hydrolysis activity and unspecific DNA binding. Elucidation of the 3D structure of the soluble deletion mutant of the conjugative coupling protein TrwB, TrwBΔN70, provided the basis for further mutagenesis studies rendering interesting insights into the structure–function of these proteins. Their key role as couplers between substrate and transporter provides biotechnological potential as targets for anti-virulence strategies, as well as for customization of substrate delivery through heterologous secretion systems.

Keywords

Bacterial conjugation Pathogenicity Type IV secretion systems Coupling proteins DNA transfer 

Notes

Acknowledgements

Work in ML laboratory is funded by grant BIO2013-46414-P from the Spanish Ministry of Economy and Competitiveness (MINECO) and grant IDEAS211LLOS from the Spanish Association Against Cancer (AECC). We are grateful to Gorka Lasso and Delfina Larrea for Fig. 1, Itxaso Álvarez for Fig. 2 and help with Tables 1 and 2, and Héctor de Paz for help with Fig. 3.

References

  1. Abajy MY, Kopec J, Schiwon K, Burzynski M, Doring M, Bohn C, Grohmann E (2007) A Type IV-secretion-like system is required for conjugative DNA transport of broad-host-range plasmid pIP501 in Gram-positive bacteria. J Bacteriol 189(6):2487–2496.  https://doi.org/10.1128/JB.01491-06CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alperi A, Larrea D, Fernandez-Gonzalez E, Dehio C, Zechner EL, Llosa M (2013) A translocation motif in relaxase TrwC specifically affects recruitment by its conjugative type IV secretion system. J Bacteriol 195(22):4999–5006.  https://doi.org/10.1128/JB.00367-13CrossRefPubMedPubMedCentralGoogle Scholar
  3. Alvarez-Martínez CE, Christie PJ (2009) Biological diversity of prokaryotic type IV secretion systems. Microbiol Mol Biol Rev 73(4):775–808CrossRefGoogle Scholar
  4. Atmakuri K, Cascales E, Christie PJ (2004) Energetic components VirD4, VirB11 and VirB4 mediate early DNA transfer reactions required for bacterial type IV secretion. Mol Microbiol 54(5):1199–1211CrossRefGoogle Scholar
  5. Bauer T, Rosch T, Itaya M, Graumann PL (2011) Localization pattern of conjugation machinery in a Gram-positive bacterium. J Bacteriol 193(22):6244–6256.  https://doi.org/10.1128/JB.00175-11CrossRefPubMedPubMedCentralGoogle Scholar
  6. Beranek A, Zettl M, Lorenzoni K, Schauer A, Manhart M, Koraimann G (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(20):6999–7006CrossRefGoogle Scholar
  7. Berry TM, Christie PJ (2011) Caught in the act: the dialogue between bacteriophage R17 and the type IV secretion machine of plasmid R1. Mol Microbiol 82(5):1039–1043CrossRefGoogle Scholar
  8. Buscher BA, Conover GM, Miller JL, Vogel SA, Meyers SN, Isberg RR, Vogel JP (2005) The DotL protein, a member of the TraG-coupling protein family, is essential for viability of Legionella pneumophila strain Lp02. J Bacteriol 187(9):2927–2938.  https://doi.org/10.1128/JB.187.9.2927-2938.2005CrossRefPubMedPubMedCentralGoogle Scholar
  9. Cabezón E, Sastre JI, de la Cruz F (1997) Genetic evidence of a coupling role for the TraG protein family in bacterial conjugation. Mol Gen Genet 254(4):400–406CrossRefGoogle Scholar
  10. Cabezon E, de la Cruz F (2006) TrwB: an F(1)-ATPase-like molecular motor involved in DNA transport during bacterial conjugation. Res Microbiol 157(4):299–305CrossRefGoogle Scholar
  11. Cabezon E, Lanza VF, Arechaga I (2011) Membrane-associated nanomotors for macromolecular transport. Curr Opin Biotechnol 23(4):537–544.  https://doi.org/10.1016/j.copbio.2011.11.031CrossRefPubMedGoogle Scholar
  12. Cascales E, Christie PJ (2004a) Definition of a bacterial type IV secretion pathway for a DNA substrate. Science 304(5674):1170–1173CrossRefGoogle Scholar
  13. Cascales E, Christie PJ (2004b) Agrobacterium VirB10, an ATP energy sensor required for type IV secretion. Proc Natl Acad Sci USA 101(49):17228–17233CrossRefGoogle Scholar
  14. Cascales E, Atmakuri K, Sarkar MK, Christie PJ (2013) DNA substrate-induced activation of the Agrobacterium VirB/VirD4 type IV secretion system. J Bacteriol 195(11):2691–2704.  https://doi.org/10.1128/JB.00114-13CrossRefPubMedPubMedCentralGoogle Scholar
  15. Casu B, Smart J, Hancock MA, Smith M, Sygusch J, Baron C (2016) Structural analysis and inhibition of TraE from the pKM101 type IV secretion system. J Biol Chem 291(45):23817–23829.  https://doi.org/10.1074/jbc.M116.753327CrossRefPubMedPubMedCentralGoogle Scholar
  16. Chen Y, Zhang X, Manias D, Yeo HJ, Dunny GM, Christie PJ (2008) Enterococcus faecalis PcfC, a spatially-localized substrate receptor for type IV secretion of the pCF10 transfer intermediate. J Bacteriol 190(10):3632–3645.  https://doi.org/10.1128/JB.01999-07CrossRefPubMedPubMedCentralGoogle Scholar
  17. Christie PJ (2016) The mosaic type IV secretion systems. EcoSal Plus.  https://doi.org/10.1128/ecosalplus.ESP-0020-2015CrossRefPubMedPubMedCentralGoogle Scholar
  18. Christie PJ (2017) Structural biology: loading T4SS substrates. Nat Microbiol 2:17125.  https://doi.org/10.1038/nmicrobiol.2017.125CrossRefPubMedGoogle Scholar
  19. Christie PJ, Whitaker N, Gonzalez-Rivera C (2014) Mechanism and structure of the bacterial type IV secretion systems. Biochim Biophys Acta 1843(8):1578–1591.  https://doi.org/10.1016/j.bbamcr.2013.12.019CrossRefPubMedPubMedCentralGoogle Scholar
  20. de Paz HD, Sangari FJ, Bolland S, Garcia-Lobo JM, Dehio C, de la Cruz F, Llosa M (2005) Functional interactions between type IV secretion systems involved in DNA transfer and virulence. Microbiology 151(Pt 11):3505–3516CrossRefGoogle Scholar
  21. de Paz HD, Larrea D, Zunzunegui S, Dehio C, de la Cruz F, Llosa M (2010) Functional dissection of the conjugative coupling protein TrwB. J Bacteriol 192(11):2655–2669CrossRefGoogle Scholar
  22. Disqué-Kochem C, Dreiseikelmann B (1997) The cytoplasmic DNA-binding protein TraM binds to the inner membrane protein TraD in vitro. J Bacteriol 179:6133–6137CrossRefGoogle Scholar
  23. Draper O, César CE, Machón C, de la Cruz F, Llosa M (2005) Site-specific recombinase and integrase activities of a conjugative relaxase in recipient cells. Proc Natl Acad Sci USA 102(45):16385–16390CrossRefGoogle Scholar
  24. Fernández-González E, de Paz HD, Alperi A, Agúndez L, Faustmann M, Sangari FJ, Dehio C, Llosa M (2011) Transfer of R388 derivatives by a pathogenesis-associated type IV secretion system into both bacteria and human cells. J Bacteriol 193(22):6257–6265CrossRefGoogle Scholar
  25. Garcillan-Barcia MP, Francia MV, de la Cruz F (2009) The diversity of conjugative relaxases and its application in plasmid classification. FEMS Microbiol Rev 33(3):657–687CrossRefGoogle Scholar
  26. Gilmour MW, Gunton JE, Lawley TD, Taylor DE (2003) Interaction between the IncHI1 plasmid R27 coupling protein and type IV secretion system: TraG associates with the coiled-coil mating pair formation protein TrhB. Mol Microbiol 49(1):105–116CrossRefGoogle Scholar
  27. Gomis-Rüth FX, Moncalián G, Pérez-Luque R, González A, Cabezón E, de la Cruz F, Coll M (2001) The bacterial conjugation protein TrwB resembles ring helicases and F1-ATPase. Nature 409(6820):637–641CrossRefGoogle Scholar
  28. Gonzalez-Rivera C, Bhatty M, Christie PJ (2016) Mechanism and function of type IV secretion during Infection of the human host. Microbiol Spectr.  https://doi.org/10.1128/microbiolspec.VMBF-0024-2015CrossRefPubMedPubMedCentralGoogle Scholar
  29. Grohmann E, Goessweiner-Mohr N, Brantl S (2016) DNA-binding proteins regulating pIP501 transfer and replication. Front Mol Biosci 3:42.  https://doi.org/10.3389/fmolb.2016.00042CrossRefPubMedPubMedCentralGoogle Scholar
  30. Grohmann E, Christie PJ, Waksman G, Backert S (2018) Type IV secretion in Gram-negative and Gram-positive bacteria. Mol Microbiol 107:455–471.  https://doi.org/10.1111/mmi.13896CrossRefGoogle Scholar
  31. Gruber CJ, Lang S, Rajendra VK, Nuk M, Raffl S, Schildbach JF, Zechner EL (2016) Conjugative DNA transfer is enhanced by plasmid R1 partitioning proteins. Front Mol Biosci 3:32.  https://doi.org/10.3389/fmolb.2016.00032CrossRefPubMedPubMedCentralGoogle Scholar
  32. Guglielmini J, de la Cruz F, Rocha EP (2013) Evolution of conjugation and type IV secretion systems. Mol Biol Evol 30(2):315–331. mss221 [pii].  https://doi.org/10.1093/molbev/mss221
  33. Gunton JE, Gilmour MW, Alonso G, Taylor DE (2005) Subcellular localization and functional domains of the coupling protein, TraG, from IncHI1 plasmid R27. Microbiology 151(Pt 11):3549–3561CrossRefGoogle Scholar
  34. Gunton JE, Gilmour MW, Baptista KP, Lawley TD, Taylor DE (2007) Interaction between the co-inherited TraG coupling protein and the TraJ membrane-associated protein of the H-plasmid conjugative DNA transfer system resembles chromosomal DNA translocases. Microbiology 153(Pt 2):428–441.  https://doi.org/10.1099/mic.0.2006/001297-0CrossRefPubMedGoogle Scholar
  35. Guo M, Jin S, Sun D, Hew CL, Pan SQ (2007) Recruitment of conjugative DNA transfer substrate to Agrobacterium type IV secretion apparatus. Proc Natl Acad Sci USA 104(50):20019–20024.  https://doi.org/10.1073/pnas.0701738104CrossRefPubMedPubMedCentralGoogle Scholar
  36. Guzmán-Herrador DL, Steiner S, Alperi A, González-Prieto C, Roy CR, Llosa M (2017) DNA delivery and genomic integration into mammalian target cells through type IV A and B secretion systems of human pathogens. Front Microbiol 8:1503.  https://doi.org/10.3389/fmicb.2017.01503CrossRefPubMedPubMedCentralGoogle Scholar
  37. Hamilton CM, Lee H, Li PL, Cook DM, Piper KR, von Bodman SB, Lanka E, Ream W, Farrand SK (2000) TraG from RP4 and TraG and VirD4 from Ti plasmids confer relaxosome specificity to the conjugal transfer system of pTiC58. J Bacteriol 182(6):1541–1548CrossRefGoogle Scholar
  38. Hormaeche I, Alkorta I, Moro F, Valpuesta JM, Goñi FM, de la Cruz F (2002) Purification and properties of TrwB, a hexameric, ATP-binding integral membrane protein essential for R388 plasmid conjugation. J Biol Chem 277(48):46456–46462CrossRefGoogle Scholar
  39. Hormaeche I, Iloro I, Arrondo JL, Goni FM, de la Cruz F, Alkorta I (2004) Role of the transmembrane domain in the stability of TrwB, an integral protein involved in bacterial conjugation. The J Biol Chem 279(12):10955–10961CrossRefGoogle Scholar
  40. Hormaeche I, Segura RL, Vecino AJ, Goni FM, de la Cruz F, Alkorta I (2006) The transmembrane domain provides nucleotide binding specificity to the bacterial conjugation protein TrwB. FEBS Lett 580(13):3075–3082CrossRefGoogle Scholar
  41. Jurik A, Hausser E, Kutter S, Pattis I, Prassl S, Weiss E, Fischer W (2010) The coupling protein Cagβ and its interaction partner CagZ are required for type IV secretion of the Helicobacter pylori CagA protein. Infect Immun 78(12):5244–5251. IAI.00796-10 [pii].  https://doi.org/10.1128/iai.00796-10CrossRefGoogle Scholar
  42. Kumar RB, Das A (2002) Polar location and functional domains of the Agrobacterium tumefaciens DNA transfer protein VirD4. Mol Microbiol 43(6):1523–1532CrossRefGoogle Scholar
  43. Kwak MJ, Kim JD, Kim H, Kim C, Bowman JW, Kim S, Joo K, Lee J, Jin KS, Kim YG, Lee NK, Jung JU, Oh BH (2017) Architecture of the type IV coupling protein complex of Legionella pneumophila. Nat Microbiol 2:17114.  https://doi.org/10.1038/nmicrobiol.2017.114CrossRefGoogle Scholar
  44. Lai EM, Chesnokova O, Banta LM, Kado CI (2000) Genetic and environmental factors affecting T-pilin export and T-pilus biogenesis in relation to flagellation of Agrobacterium tumefaciens. J Bacteriol 182(13):3705–3716CrossRefGoogle Scholar
  45. Lang S, Kirchberger PC, Gruber CJ, Redzej A, Raffl S, Zellnig G, Zangger K, Zechner EL (2011) An activation domain of plasmid R1 TraI protein delineates stages of gene transfer initiation. Mol Microbiol 82(5):1071–1085CrossRefGoogle Scholar
  46. Lang S, Zechner EL (2012) General requirements for protein secretion by the F-like conjugation system R1. Plasmid 67(2):128–138. S0147-619X(12)00002-9 [pii].  https://doi.org/10.1016/j.plasmid.2011.12.014CrossRefGoogle Scholar
  47. Larrea D, de Paz HD, Arechaga I, de la Cruz F, Llosa M (2013) Structural independence of conjugative coupling protein TrwB from its type IV secretion machinery. Plasmid 70(1):146–153.  https://doi.org/10.1016/j.plasmid.2013.03.006CrossRefPubMedGoogle Scholar
  48. Larrea D, de Paz HD, Matilla I, Guzman-Herrador DL, Lasso G, de la Cruz F, Cabezon E, Llosa M (2017) Substrate translocation involves specific lysine residues of the central channel of the conjugative coupling protein TrwB. Mol Genet Genomics 292(5):1037–1049.  https://doi.org/10.1007/s00438-017-1331-3CrossRefPubMedGoogle Scholar
  49. Lawley TD, Gilmour MW, Gunton JE, Standeven LJ, Taylor DE (2002) Functional and mutational analysis of conjugative transfer region 1 (Tra1) from the IncHI1 plasmid R27. J Bacteriol 184(8):2173–2180CrossRefGoogle Scholar
  50. Li F, Alvarez-Martinez C, Chen Y, Choi KJ, Yeo HJ, Christie PJ (2012) Enterococcus faecalis PrgJ, a VirB4-like ATPase, mediates pCF10 conjugative transfer through substrate binding. J Bacteriol 194(15):4041–4051. JB.00648-12 [pii].  https://doi.org/10.1128/jb.00648-12CrossRefGoogle Scholar
  51. Low HH, Gubellini F, Rivera-Calzada A, Braun N, Connery S, Dujeancourt A, Lu F, Redzej A, Fronzes R, Orlova EV, Waksman G (2014) Structure of a type IV secretion system. Nature 508(7497):550–553.  https://doi.org/10.1038/nature13081CrossRefPubMedPubMedCentralGoogle Scholar
  52. Lu J, Frost LS (2005) Mutations in the C-terminal region of TraM provide evidence for in vivo TraM-TraD interactions during F-plasmid conjugation. J Bacteriol 187(14):4767–4773CrossRefGoogle Scholar
  53. Lu J, Wong JJ, Edwards RA, Manchak J, Frost LS, Glover JN (2008) Structural basis of specific TraD-TraM recognition during F plasmid-mediated bacterial conjugation. Mol Microbiol 70(1):89–99CrossRefGoogle Scholar
  54. Llosa M, Gomis-Rüth F-X, Coll M, de la Cruz F (2002) Bacterial conjugation: a two-step mechanism for DNA transport. Mol Microbiol 45:1–8CrossRefGoogle Scholar
  55. Llosa M, Zunzunegui S, de la Cruz F (2003) Conjugative coupling proteins interact with cognate and heterologous VirB10-like proteins while exhibiting specificity for cognate relaxosomes. Proc Natl Acad Sci USA 100(18):10465–10470CrossRefGoogle Scholar
  56. Llosa M, Schroder G, Dehio C (2012) New perspectives into bacterial DNA transfer to human cells. Trends Microbiol 20(8):355–359. S0966-842X(12)00100-X [pii].  https://doi.org/10.1016/j.tim.2012.05.008CrossRefGoogle Scholar
  57. Maizels N, Gray LT (2013) The G4 genome. PLoS Genet 9(4):e1003468.  https://doi.org/10.1371/journal.pgen.1003468CrossRefPubMedPubMedCentralGoogle Scholar
  58. Matilla I, Alfonso C, Rivas G, Bolt EL, de la Cruz F, Cabezon E (2010) The conjugative DNA translocase TrwB is a structure-specific DNA-binding protein. J Biol Chem 285(23):17537–17544.  https://doi.org/10.1074/jbc.M109.084137CrossRefPubMedPubMedCentralGoogle Scholar
  59. Meyer R (2015) Mapping type IV secretion signals on the primase encoded by the broad-host-range plasmid R1162 (RSF1010). J Bacteriol 197(20):3245–3254.  https://doi.org/10.1128/JB.00443-15CrossRefPubMedPubMedCentralGoogle Scholar
  60. Middleton R, Sjolander K, Krishnamurthy N, Foley J, Zambryski P (2005) Predicted hexameric structure of the Agrobacterium VirB4 C terminus suggests VirB4 acts as a docking site during type IV secretion. Proc Natl Acad Sci USA 102(5):1685–1690CrossRefGoogle Scholar
  61. Mihajlovic S, Lang S, Sut MV, Strohmaier H, Gruber CJ, Koraimann G, Cabezon E, Moncalian G, de la Cruz F, Zechner EL (2009) Plasmid R1 conjugative DNA processing is regulated at the coupling protein interface. J Bacteriol 191(22):6877–6887CrossRefGoogle Scholar
  62. Moncalian G, Cabezon E, Alkorta I, Valle M, Moro F, Valpuesta JM, Goni FM, de la Cruz F (1999) Characterization of ATP and DNA binding activities of TrwB, the coupling protein essential in plasmid R388 conjugation. J Biol Chem 274(51):36117–36124CrossRefGoogle Scholar
  63. Mulkidjanian AY, Makarova KS, Galperin MY, Koonin EV (2007) Inventing the dynamo machine: the evolution of the F-type and V-type ATPases. Nat Rev Microbiol 5(11):892–899.  https://doi.org/10.1038/nrmicro1767CrossRefPubMedGoogle Scholar
  64. Parsons JA, Bannam TL, Devenish RJ, Rood JI (2007) TcpA, an FtsK/SpoIIIE homolog, is essential for transfer of the conjugative plasmid pCW3 in Clostridium perfringens. J Bacteriol 189(21):7782–7790CrossRefGoogle Scholar
  65. Pena A, Matilla I, Martin-Benito J, Valpuesta JM, Carrascosa JL, de la Cruz F, Cabezon E, Arechaga I (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(47):39925–39932.  https://doi.org/10.1074/jbc.M112.413849CrossRefPubMedPubMedCentralGoogle Scholar
  66. Rangrez AY, Abajy MY, Keller W, Shouche Y, Grohmann E (2010) Biochemical characterization of three putative ATPases from a new type IV secretion system of Aeromonas veronii plasmid pAC3249A. BMC Biochem 11:10.  https://doi.org/10.1186/1471-2091-11-10CrossRefPubMedPubMedCentralGoogle Scholar
  67. Redzej A, Ukleja M, Connery S, Trokter M, Felisberto-Rodrigues C, Cryar A, Thalassinos K, Hayward RD, Orlova EV, Waksman G (2017) Structure of a VirD4 coupling protein bound to a VirB type IV secretion machinery. EMBO J Sep 18 pii: e201796629.  https://doi.org/10.15252/embj.201796629
  68. Rennoll-Bankert KE, Rahman MS, Gillespie JJ, Guillotte ML, Kaur SJ, Lehman SS, Beier-Sexton M, Azad AF (2015) Which way in? The RalF Arf-GEF orchestrates Rickettsia host cell invasion. PLoS Pathog 11(8):e1005115.  https://doi.org/10.1371/journal.ppat.1005115CrossRefPubMedPubMedCentralGoogle Scholar
  69. Rikihisa Y, Lin M, Niu H (2010) Type IV secretion in the obligatory intracellular bacterium Anaplasma phagocytophilum. Cell Microbiol 12(9):1213–1221.  https://doi.org/10.1111/j.1462-5822.2010.01500.xCrossRefPubMedPubMedCentralGoogle Scholar
  70. Ripoll-Rozada J, Zunzunegui S, de la Cruz F, Arechaga I, Cabezon E (2013) Functional interactions of VirB11 traffic ATPases with VirB4 and VirD4 molecular motors in type IV secretion systems. J Bacteriol 195(18):4195–4201.  https://doi.org/10.1128/JB.00437-13CrossRefPubMedPubMedCentralGoogle Scholar
  71. Ripoll-Rozada J, Garcia-Cazorla Y, Getino M, Machon C, Sanabria-Rios D, de la Cruz F, Cabezon E, Arechaga I (2016) Type IV traffic ATPase TrwD as molecular target to inhibit bacterial conjugation. Mol Microbiol 100(5):912–921.  https://doi.org/10.1111/mmi.13359CrossRefPubMedPubMedCentralGoogle Scholar
  72. Sastre JI, Cabezón E, de la Cruz F (1998) The carboxyl terminus of protein TraD adds specificity and efficiency to F-plasmid conjugative transfer. J Bacteriol 180(22):6039–6042PubMedPubMedCentralGoogle Scholar
  73. Schröder G, Krause S, Zechner EL, Traxler B, Yeo HJ, Lurz R, Waksman G, Lanka E (2002) TraG-like proteins of DNA transfer systems and of the Helicobacter pylori type IV secretion system: inner membrane gate for exported substrates? J Bacteriol 184(10):2767–2779CrossRefGoogle Scholar
  74. Schröder G, Lanka E (2003) TraG-like proteins of type IV secretion systems: functional dissection of the multiple activities of TraG (RP4) and TrwB (R388). J Bacteriol 185(15):4371–4381CrossRefGoogle Scholar
  75. Schröder G, Schülein R, Quebatte M, Dehio C (2011) Conjugative DNA transfer into human cells by the VirB/VirD4 type IV secretion system of the bacterial pathogen Bartonella henselae. Proc Natl Acad Sci USA 108(35):14643–14648.  https://doi.org/10.1073/pnas.1019074108CrossRefPubMedPubMedCentralGoogle Scholar
  76. Segura RL, Aguila-Arcos S, Ugarte-Uribe B, Vecino AJ, de la Cruz F, Goni FM, Alkorta I (2013) The transmembrane domain of the T4SS coupling protein TrwB and its role in protein-protein interactions. Biochim Biophys Acta 1828(9):2015–2025.  https://doi.org/10.1016/j.bbamem.2013.05.022CrossRefPubMedGoogle Scholar
  77. Segura RL, Aguila-Arcos S, Ugarte-Uribe B, Vecino AJ, de la Cruz F, Goni FM, Alkorta I (2014) Subcellular location of the coupling protein TrwB and the role of its transmembrane domain. Biochim Biophys Acta 1838(1 Pt B):223–230.  https://doi.org/10.1016/j.bbamem.2013.08.016CrossRefGoogle Scholar
  78. Smillie C, Garcillan-Barcia MP, Francia MV, Rocha EP, de la Cruz F (2010) Mobility of plasmids. Microbiol Mol Biol Rev 74(3):434–452.  https://doi.org/10.1128/MMBR.00020-10CrossRefPubMedPubMedCentralGoogle Scholar
  79. Steen JA, Bannam TL, Teng WL, Devenish RJ, Rood JI (2009) The putative coupling protein TcpA interacts with other pCW3-encoded proteins to form an essential part of the conjugation complex. J Bacteriol 191(9):2926–2933CrossRefGoogle Scholar
  80. Sutherland MC, Nguyen TL, Tseng V, Vogel JP (2012) The Legionella IcmSW complex directly interacts with DotL to mediate translocation of adaptor-dependent substrates. PLoS Pathog 8(9):e1002910.  https://doi.org/10.1371/journal.ppat.1002910CrossRefPubMedPubMedCentralGoogle Scholar
  81. Tato I, Zunzunegui S, de la Cruz F, Cabezón E (2005) TrwB, the coupling protein involved in DNA transport during bacterial conjugation, is a DNA-dependent ATPase. Proc Natl Acad Sci USA 102(23):8156–8161CrossRefGoogle Scholar
  82. Tato I, Matilla I, Arechaga I, Zunzunegui S, de la Cruz F, Cabezon E (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(35):25569–25576CrossRefGoogle Scholar
  83. Vecino AJ, Segura RL, Ugarte-Uribe B, Aguila S, Hormaeche I, de la Cruz F, Goni FM, Alkorta I (2010) Reconstitution in liposome bilayers enhances nucleotide binding affinity and ATP-specificity of TrwB conjugative coupling protein. Biochim Biophys Acta 1798(11):2160–2169. S0005-2736(10)00239-7 [pii].  https://doi.org/10.1016/j.bbamem.2010.07.005CrossRefGoogle Scholar
  84. Vecino AJ, de la Arada I, Segura RL, Goni FM, de la Cruz F, Arrondo JL, Alkorta I (2011) Membrane insertion stabilizes the structure of TrwB, the R388 conjugative plasmid coupling protein. Biochim Biophys Acta 1808(4):1032–1039. S0005-2736(10)00460-8 [pii].  https://doi.org/10.1016/j.bbamem.2010.12.025CrossRefGoogle Scholar
  85. Vecino AJ, Segura Rde L, de la Arada I, de la Cruz F, Goni FM, Arrondo JL, Alkorta I (2012) Deletion of a single helix from the transmembrane domain causes large changes in membrane insertion properties and secondary structure of the bacterial conjugation protein TrwB. Biochim Biophys Acta 1818(12):3158–3166.  https://doi.org/10.1016/j.bbamem.2012.08.015CrossRefPubMedGoogle Scholar
  86. Vergunst AC, van Lier MC, den Dulk-Ras A, Grosse Stuve TA, Ouwehand A, Hooykaas PJ (2005) Positive charge is an important feature of the C-terminal transport signal of the VirB/D4-translocated proteins of Agrobacterium. Proc Natl Acad Sci USA 102(3):832–837CrossRefGoogle Scholar
  87. Wallden K, Williams R, Yan J, Lian PW, Wang L, Thalassinos K, Orlova EV, Waksman G (2012) Structure of the VirB4 ATPase, alone and bound to the core complex of a type IV secretion system. Proc Natl Acad Sci USA 109(28):11348–11353. 1201428109 [pii].  https://doi.org/10.1073/pnas.1201428109CrossRefGoogle Scholar
  88. Whitaker N, Chen Y, Jakubowski SJ, Sarkar MK, Li F, Christie PJ (2015) The all-alpha domains of coupling proteins from the Agrobacterium tumefaciens VirB/VirD4 and Enterococcus faecalis pCF10-encoded type IV secretion systems confer specificity to binding of cognate DNA substrates. J Bacteriol 197(14):2335–2349.  https://doi.org/10.1128/JB.00189-15CrossRefPubMedPubMedCentralGoogle Scholar
  89. Whitaker N, Berry TM, Rosenthal N, Gordon JE, Gonzalez-Rivera C, Sheehan KB, Truchan HK, VieBrock L, Newton IL, Carlyon JA, Christie PJ (2016) Chimeric coupling proteins mediate transfer of heterologous type IV effectors through the Escherichia coli pKM101-encoded conjugation machine. J Bacteriol 198(19):2701–2718.  https://doi.org/10.1128/JB.00378-16CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Departamento de Biología MolecularUniversidad de Cantabria (UC), and Instituto de Biomedicina y Biotecnología de Cantabria (IBBTEC), UC-CSIC-SODERCANSantanderSpain
  2. 2.Departamento de Bioquímica y Biología Molecular (UPV/EHU)Instituto Biofisika (UPV/EHU, CSIC)LeioaSpain

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