Subcellular location of the coupling protein TrwB and the role of its transmembrane domain

Biochimica et Biophysica Acta - Biomembranes

Volumn 1838, Issue 1 PARTB, 2014, Pages 223-230

  Segura, Rosa L ^a   Águila Arcos, Sandra ^a   Ugarte Uribe, Begoña ^a   Vecino, Ana J ^a   De La Cruz, Fernando ^b   Goñi, Félix M ^a   Alkorta, Itziar ^a  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^b UNIVERSITY OF CANTABRIA   (Spain)

Author keywords

Bacterial conjugation; Coupling protein; Plasmid R388; Protein cell location; Type IV secretion system

Indexed keywords

BINDING PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; PROTEIN TRWB; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL STRAIN; BACTERIUM CONJUGATION; CELLULAR DISTRIBUTION; CYTOPLASM; CYTOPLASMIC DOMAIN; IMMUNOFLUORESCENCE; IMMUNOFLUORESCENCE MICROSCOPY; MUTANT; PLASMID; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; TRANSMEMBRANE DOMAIN;

EID: 84887866115     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2013.08.016     Document Type: Article

References (56)

1. C.E. Alvarez-Martinez, and P.J. Christie Biological diversity of prokaryotic type IV secretion systems Microbiol. Mol. Biol. Rev. 73 2009 775 808
2. F. Baquero, T.M. Coque, and F. de la Cruz Ecology and evolution as targets: the need for novel eco-evo drugs and strategies to fight antibiotic resistance Antimicrob. Agents Chemother. 55 2011 3649 3660
3. E.L. Zechner, S. Lang, and J.F. Schildbach Assembly and mechanisms of bacterial type IV secretion machines Philos. Trans. R. Soc. Lond. B Biol. Sci. 367 2012 1073 1087
4. O. Draper, C.E. César, C. Machón, F. de la Cruz, and M. Llosa Site-specific recombinase and integrase activities of a conjugative relaxase in recipient cells Proc. Natl. Acad. Sci. U. S. A. 102 2005 16385 16390 (Pubitemid 41688923)
5. C.E. César, C. Machón, F. de la Cruz, and M. Llosa A new domain of conjugative relaxase TrwC responsible for efficient oriT-specific recombination on minimal target sequences Mol. Microbiol. 62 2006 984 996 (Pubitemid 44655313)
6. M.P. Garcillan-Barcia, M.V. Francia, and F. de la Cruz The diversity of conjugative relaxases and its application in plasmid classification FEMS Microbiol. Rev. 33 2009 657 687
7. E. Cabezon, and F. de la Cruz TrwB: an F(1)-ATPase-like molecular motor involved in DNA transport during bacterial conjugation Res. Microbiol. 157 2006 299 305
8. K. Wallden, A. Rivera-Calzada, and G. Waksman Type IV secretion systems: versatility and diversity in function Cell. Microbiol. 12 2010 1203 1212
9. L. Terradot, R. Bayliss, C. Oomen, G.A. Leonard, C. Baron, and G. Waksman 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. U. S. A. 102 2005 4596 4601 (Pubitemid 40397157)
10. R. Bayliss, R. Harris, L. Coutte, A. Monier, R. Fronzes, P.J. Christie, P.C. Driscoll, and G. Waksman NMR structure of a complex between the VirB9/VirB7 interaction domains of the pKM101 type IV secretion system Proc. Natl. Acad. Sci. U. S. A. 104 2007 1673 1678 (Pubitemid 46214649)
11. V. Chandran, R. Fronzes, S. Duquerroy, N. Cronin, J. Navaza, and G. Waksman Structure of the outer membrane complex of a type IV secretion system Nature 462 2009 1011 1015
12. R. Fronzes, E. Schäfer, L. Wang, H.R. Saibil, E.V. Orlova, and G. Waksman Structure of a type IV secretion system core complex Science 323 2009 266 268
13. R.B. Kumar, Y.H. Xie, and A. Das Subcellular localization of the Agrobacterium tumefaciens T-DNA transport pore proteins: VirB8 is essential for the assembly of the transport pore Mol. Microbiol. 36 2000 608 617 (Pubitemid 30258845)
14. R.B. Kumar, and A. Das Polar location and functional domains of the Agrobacterium tumefaciens DNA transfer protein VirD4 Mol. Microbiol. 43 2002 1523 1532 (Pubitemid 34595543)
15. K. Atmakuri, Z. Ding, and P.J. Christie VirE2, a type IV secretion substrate, interacts with the VirD4 transfer protein at cell poles of Agrobacterium tumefaciens Mol. Microbiol. 49 2003 1699 1713 (Pubitemid 37153526)
16. J.E. Gunton, M.W. Gilmour, G. Alonso, and D.E. Taylor Subcellular localization and functional domains of the coupling protein, TraG, from IncHI1 plasmid R27 Microbiology 151 2005 3549 3561 (Pubitemid 41632068)
17. P.K. Judd, R.B. Kumar, and A. Das The type IV secretion apparatus protein VirB6 of Agrobacterium tumefaciens localizes to a cell pole Mol. Microbiol. 55 2005 115 124 (Pubitemid 40127889)
18. P.K. Judd, R.B. Kumar, and A. Das Spatial location and requirements for the assembly of the Agrobacterium tumefaciens type IV secretion apparatus Proc. Natl. Acad. Sci. U. S. A. 102 2005 11498 11503 (Pubitemid 41153848)
19. M.W. Gilmour, J.E. Gunton, T.D. Lawley, and D.E. Taylor 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 2003 105 116 (Pubitemid 36792007)
20. F.X. Gomis-Rüth, F. de la Cruz, and M. Coll Structure and role of coupling proteins in conjugal DNA transfer Res. Microbiol. 153 2002 199 204 (Pubitemid 34327892)
21. M. Llosa, and F. de la Cruz Bacterial conjugation: a potential tool for genetic engineering Res. Microbiol. 156 2005 1 6 (Pubitemid 40075583)
22. A. Das, and Y.H. Xie Construction of transposon Tn3phoA: its application in defining the membrane topology of the Agrobacterium tumefaciens DNA transfer proteins Mol. Microbiol. 27 1998 405 414 (Pubitemid 28035264)
23. G. Schröder, S. Krause, E.L. Zechner, B. Traxler, H.J. Yeo, R. Lurz, G. Waksman, and E. Lanka 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 2002 2767 2779 (Pubitemid 34457044)
24. G. Moncalián, E. Cabezón, I. Alkorta, M. Valle, F. Moro, J.M. Valpuesta, F.M. Goñi, and F. de la Cruz Characterization of ATP and DNA binding activities of TrwB, the coupling protein essential in plasmid R388 conjugation J. Biol. Chem. 274 1999 36117 36124
25. F.X. Gomis-Rüth, G. Moncalián, R. Pérez-Luque, A. González, E. Cabezón, F. de la Cruz, and M. Coll The bacterial conjugation protein TrwB resembles ring helicases and F1-ATPase Nature 409 2001 637 641 (Pubitemid 32154818)
26. F.X. Gomis-Rüth, G. Moncalián, F. Cruz, and M. Coll 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 2002 7556 7566 (Pubitemid 34953154)
27. I. Hormaeche, I. Alkorta, F. Moro, J.M. Valpuesta, F.M. Goñi, and F. de la Cruz Purification and properties of TrwB, a hexameric, ATP-binding integral membrane protein essential for R388 plasmid conjugation J. Biol. Chem. 277 2002 46456 46462 (Pubitemid 35417641)
28. I. Tato, S. Zunzunegui, F. de la Cruz, and E. Cabezon TrwB, the coupling protein involved in DNA transport during bacterial conjugation, is a DNA-dependent ATPase Proc. Natl. Acad. Sci. U. S. A. 102 2005 8156 8161 (Pubitemid 40800059)
29. I. Hormaeche, R.L. Segura, A.J. Vecino, F.M. Goñi, F. de la Cruz, and I. Alkorta The transmembrane domain provides nucleotide binding specificity to the bacterial conjugation protein TrwB FEBS Lett. 580 2006 3075 3082 (Pubitemid 43729655)
30. I. Tato, I. Matilla, I. Arechaga, S. Zunzunegui, F. de la Cruz, and E. Cabezon 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 2007 25569 25576 (Pubitemid 47372773)
31. I. Matilla, C. Alfonso, G. Rivas, E.L. Bolt, F. de la Cruz, and E. Cabezon The conjugative DNA translocase TrwB is a structure-specific DNA-binding protein J. Biol. Chem. 285 2010 17537 17544
32. A.J. Vecino, R.L. Segura, B. Ugarte-Uribe, S. Aguila, I. Hormaeche, F. de la Cruz, F.M. Goñi, and I. Alkorta Reconstitution in liposome bilayers enhances nucleotide binding affinity and ATP-specificity of TrwB conjugative coupling protein Biochim. Biophys. Acta 1798 2010 2160 2169
33. I. Hormaeche, I. Iloro, J.L. Arrondo, F.M. Goñi, F. de la Cruz, and I. Alkorta Role of the transmembrane domain in the stability of TrwB, an integral protein involved in bacterial conjugation J. Biol. Chem. 279 2004 10955 10961 (Pubitemid 38401586)
34. A.J. Vecino, I. de la Arada, R.L. Segura, F. de la Cruz, F.M. Goñi, and I. Alkorta Membrane insertion stabilizes the structure of TrwB the R388 conjugative plasmid coupling protein Biochim. Biophys. Acta 1808 2011 1032 1039
35. A.J. Vecino, R.L. Segura, I. de la Arada, F. Cruz, F.M. Goñi, J.L.R. Arrondo, and I. Alkorta 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 2012 3158 3166
36. S.G. Grant, J. Jessee, F.R. Bloom, and D. Hanahan Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants Proc. Natl. Acad. Sci. U. S. A. 87 1990 4645 4649
37. F. de la Cruz, and J. Grinsted Genetic and molecular characterization of Tn21, a multiple resistance transposon from R100.1 J. Bacteriol. 151 1982 222 228 (Pubitemid 12022327)
38. B. Miroux, and J.E. Walker Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels J. Mol. Biol. 260 1996 289 298 (Pubitemid 26254109)
39. F.W. Studier, and B.A. Moffatt Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes J. Mol. Biol. 189 1986 113 130
40. G.S. Waldo, B.M. Standish, J. Berendzen, and T.C. Terwilliger Rapid protein-folding assay using green fluorescent protein Nat. Biotechnol. 17 1999 691 695 (Pubitemid 29316148)
41. N. Datta, and R.W. Hedges Trimethoprim resistance conferred by W plasmids in Enterobacteriaceae J. Gen. Microbiol. 72 1972 349 355
42. M. Llosa, S. Bolland, and F. de la Cruz Genetic organization of the conjugal DNA processing region of the IncW plasmid R388 J. Mol. Biol. 235 1994 448 464 (Pubitemid 24063571)
43. J. Sambrook, E.F. Fritsch, and T. Maniatis Molecular Cloning: A Laboratory Manual 1989 Cold Spring Harbor Lab. Press Plainview, New York
44. M. Llosa, S. Zunzunegui, and F. de la Cruz Conjugative coupling proteins interact with cognate and heterologous VirB10-like proteins while exhibiting specificity for cognate relaxosomes Proc. Natl. Acad. Sci. U. S. A. 100 2003 10465 10470 (Pubitemid 37071901)
45. W.L. Teng, T.L. Bannam, J.A. Parsons, and J.I. Rood Functional characterization and localization of the TcpH conjugation protein from Clostridium perfringens J. Bacteriol. 190 2008 5075 5086 (Pubitemid 351991075)
46. R.L. Segura, S. Águila-Arcos, B. Ugarte-Uribe, A.J. Vecino, F. de la Cruz, F.M. Goñi, and I. Alkorta The transmembrane domain of the T4SS coupling protein TrwB and its role in protein-protein interactions Biochim. Biophys. Acta 2013 10.1016/j.bbamem.2013.05.022
47. T. Bauer, T. Rösch, M. Itaya, and P.L. Graumann Localization pattern of conjugation machinery in a gram-positive bacterium J. Bacteriol. 193 2011 6244 6256
48. P. Mossey, A. Hudacek, and A. Das Agrobacterium tumefaciens type IV secretion protein VirB3 is an inner membrane protein and requires VirB4, VirB7, and VirB8 for stabilization J. Bacteriol. 192 2010 2830 2838
49. J. Aguilar, T.A. Cameron, J. Zupan, and P. Zambryski Membrane and core periplasmic Agrobacterium tumefaciens virulence Type IV secretion system components localize to multiple sites around the bacterial perimeter during lateral attachment to plant cells MBio 2 2011 e00218-11
50. T.A. Cameron, M. Roper, and P. Zambryski Quantitative image analysis and modeling indicate the Agrobacterium tumefaciens type IV secretion system is organized in a periodic pattern of foci PLoS One 7 2012 e42219
51. K. Atmakuri, E. Cascales, O.T. Burton, L.M. Banta, and P.J. Christie Agrobacterium ParA/MinD-like VirC1 spatially coordinates early conjugative DNA transfer reactions EMBO J. 26 2007 2540 2551 (Pubitemid 46788322)
52. J. Aguilar, J. Zupan, T.A. Cameron, and P.C. Zambryski Agrobacterium type IV secretion system and its substrates form helical arrays around the circumference of virulence-induced cells Proc. Natl. Acad. Sci. U. S. A. 107 2010 3758 3763
53. L. Shapiro, H.H. McAdams, and R. Losick Generating and exploiting polarity in bacteria Science 298 2002 1942 1946 (Pubitemid 35425241)
54. A. Nishibori, J. Kusaka, H. Hara, M. Umeda, and K. Matsumoto Phosphatidylethanolamine domains and localization of phospholipid synthases in Bacillus subtilis membranes J. Bacteriol. 187 2005 2163 2174 (Pubitemid 40316247)
55. T. Romantsov, S. Helbig, D.E. Culham, C. Gill, L. Stalker, and J.M. Wood Cardiolipin promotes polar localization of osmosensory transporter ProP in Escherichia coli Mol. Microbiol. 64 2007 1455 1465 (Pubitemid 46889896)
56. C. Guynet, A. Cuevas, G. Moncalián, and F. de la Cruz The stb operon balances the requirements for vegetative stability and conjugative transfer of plasmid R388 PLoS Genet. 7 2011 e1002073