DNA Substrate-Induced Activation of the Agrobacterium VirB/VirD4 Type IV Secretion System

Journal of Bacteriology

Volumn 195, Issue 11, 2013, Pages 2691-2704

  Cascales, Eric ^a,b   Atmakuri, Krishnamohan ^a,c   Sarkar, Mayukh K ^a   Christie, Peter J ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b CNRS and Aix Marseille University   (France)

^c Translational Health Science and Technology Institute   (India)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; DNA; PROTEIN VIRB10; PROTEIN VIRD4; PROTEIN VIRE2; PROTEIN VIRE3; PROTEIN VIRF; UNCLASSIFIED DRUG; VIRB PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CONFORMATIONAL TRANSITION; DNA TRANSFER; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN TRANSPORT; RHIZOBIUM; TYPE IV SECRETION SYSTEM;

ADENOSINE TRIPHOSPHATASES; AGROBACTERIUM TUMEFACIENS; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CONJUGATION, GENETIC; DNA MUTATIONAL ANALYSIS; DNA, BACTERIAL; DNA-BINDING PROTEINS; MEMBRANE PROTEINS; MODELS, MOLECULAR; MUTATION; PEPTIDE HYDROLASES; PLASMIDS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; VIRULENCE FACTORS;

EID: 84878001178     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00114-13     Document Type: Article

References (78)

1. Alvarez-Martinez CE, Christie PJ. 2009. Biological diversity of prokaryotic type IV secretion systems. Microbiol. Mol. Biol. Rev. 73:775-808.
2. de la Cruz F, Frost LS, Meyer RJ, Zechner EL. 2010. Conjugative DNA metabolism in Gram-negative bacteria. FEMS Microbiol. Rev. 34:18-40.
3. Zechner EL, Lang S, Schildbach JF. 2012. Assembly and mechanisms of bacterial type IV secretion machines. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367:1073-1087.
4. Wong JJ, Lu J, Glover JN. 2012. Relaxosome function and conjugation regulation in F-like plasmids-a structural biology perspective. Mol. Microbiol. 85:602-617.
5. Gomis-Ruth FX, de la Cruz F, Coll M. 2002. Structure and role of coupling proteins in conjugal DNA transfer. Res. Microbiol. 153:199-204.
6. Schroder G, Lanka E. 2005. The mating pair formation system of conjugative plasmids-a versatile secretion machinery for transfer of proteins and DNA. Plasmid 54:1-25.
7. Wallden K, Rivera-Calzada A, Waksman G. 2010. Type IV secretion systems: versatility and diversity in function. Cell. Microbiol. 12:1203-1212.
8. Gomis-Ruth FX, Coll M. 2001. Structure of TrwB, a gatekeeper in bacterial conjugation. Int. J. Biochem. Cell Biol. 33:839-843.
9. Hormaeche I, Alkorta I, Moro F, Valpuesta JM, Goni 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. 277:46456-46462.
10. Gomis-Ruth FX, Sola M, de la Cruz F, Coll M. 2004. Coupling factors in macromolecular type-IV secretion machineries. Curr. Pharm. Des. 10: 1551-1565.
11. Fronzes R, Christie PJ, Waksman G. 2009. The structural biology of type IV secretion systems. Nat. Rev. Microbiol. 7:703-714.
12. Fronzes R, Schafer E, Wang L, Saibil HR, Orlova EV, Waksman G. 2009. Structure of a type IV secretion system core complex. Science 323: 266-268.
13. Chandran V, Fronzes R, Duquerroy S, Cronin N, Navaza J, Waksman G. 2009. Structure of the outer membrane complex of a type IV secretion system. Nature 462:1011-1015.
14. Christie PJ, Atmakuri K, Krishnamoorthy V, Jakubowski S, Cascales E. 2005. Biogenesis, architecture, and function of bacterial type IV secretion systems. Annu. Rev. Microbiol. 59:451-485.
15. Sarkar MM, Husnain SI, Jakubowski SJ, Christie PJ. 2013. Isolation of bacterial type IV machine subassemblies, p 187-204. In Delcour A (ed), The bacterial cell surface: methods and protocols, methods in molecular biology. Humana Press, Inc., New York, NY.
16. Christie PJ. 2009. Structural biology: translocation chamber's secrets. Nature 462:992-994.
17. Cascales E, Christie PJ. 2004. Definition of a bacterial type IV secretion pathway for a DNA substrate. Science 304:1170-1173.
18. 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. 54:1199-1211.
19. Jakubowski SJ, Krishnamoorthy V, Cascales E, Christie PJ. 2004. Agrobacterium tumefaciens VirB6 domains direct the ordered export of a DNA substrate through a type IV secretion system. J. Mol. Biol. 341:961-977.
20. Thanassi DG, Bliska JB, Christie PJ. 2012. Surface organelles assembled by secretion systems of Gram-negative bacteria: diversity in structure and function. FEMS Microbiol. Rev. 36:1046-1082.
21. Cascales E, Christie PJ. 2004. Agrobacterium VirB10, an ATP energy sensor required for type IV secretion. Proc. Natl. Acad. Sci. U. S. A. 101: 17228-17233.
22. Banta LM, Kerr JE, Cascales E, Giuliano ME, Bailey ME, McKay C, Chandran V, Waksman G, Christie PJ. 2011. An Agrobacterium VirB10 mutation conferring a type IV secretion system gating defect. J. Bacteriol. 193:2566-2574.
23. Zhu J, Oger PM, Schrammeijer B, Hooykaas PJ, Farrand SK, Winans SC. 2000. The bases of crown gall tumorigenesis. J. Bacteriol. 182:3885-3895.
24. Van Larebeke N, Genetello C, Schell J, Schilperoort RA, Hermans AK, Van Montagu M, Hernalsteens JP. 1975. Acquisition of tumourinducing ability by non-oncogenic agrobacteria as a result of plasmid transfer. Nature 255:742-743.
25. McBride KE, Knauf VC. 1988. Genetic analysis of the virE operon of the Agrobacterium Ti plasmid pTiA6. J. Bacteriol. 170:1430-1437.
26. Fullner KJ, Lara JC, Nester EW. 1996. Pilus assembly by Agrobacterium T-DNA transfer genes. Science 273:1107-1109.
27. Stachel SE, An G, Flores C, Nester EW. 1985. A Tn3 lacZ transposon for the random generation of beta-galactosidase gene fusions: application to the analysis of gene expression in Agrobacterium. EMBO J. 4:891-898.
28. Ooms G, Hooykaas PJJ, Van Veen RJM, Van Beelen P, Regensburg-Tunik R, Schilperoort RA. 1982. Octopine Ti-plasmid deletion mutants of Agrobacterium tumefaciens with emphasis on the right side of the T-region. Plasmid 7:15-19.
29. Berger BR, Christie PJ. 1994. Genetic complementation analysis of the Agrobacterium tumefaciens virB operon: virB2 through virB11 are essential virulence genes. J. Bacteriol. 176:3646-3660.
30. Zhou XR, Christie PJ. 1997. Suppression of mutant phenotypes of the Agrobacterium tumefaciens VirB11 ATPase by overproduction of VirB proteins. J. Bacteriol. 179:5835-5842.
31. Lee LY, Gelvin SB. 2008. T-DNA binary vectors and systems. Plant Physiol. 146:325-332.
32. Cascales E, Atmakuri K, Liu Z, Binns AN, Christie PJ. 2005. Agrobacterium tumefaciens oncogenic suppressors inhibit T-DNA and VirE2 protein substrate binding to the VirD4 coupling protein. Mol. Microbiol. 58:565-579.
33. Rashkova S, Spudich GM, Christie PJ. 1997. Characterization of membrane and protein interaction determinants of the Agrobacterium tumefaciens VirB11 ATPase. J. Bacteriol. 179:583-591.
34. Fullner KJ, Nester EW. 1996. Temperature affects the T-DNA transfer machinery of Agrobacterium tumefaciens. J. Bacteriol. 178:1498-1504.
35. Beaupre CE, Bohne J, Dale EM, Binns AN. 1997. Interactions between VirB9 and VirB10 membrane proteins involved in movement of DNA from Agrobacterium tumefaciens into plant cells. J. Bacteriol. 179:78-89.
36. Stahl LE, Jacobs A, Binns AN. 1998. The conjugal intermediate of plasmid RSF1010 inhibits Agrobacterium tumefaciens virulence and VirBdependent export of VirE2. J. Bacteriol. 180:3933-3939.
37. Escudero J, Den Dulk-Ras A, Regensburg-Tuink TJ, Hooykaas PJ. 2003. VirD4-independent transformation by CloDF13 evidences an unknown factor required for the genetic colonization of plants via Agrobacterium. Mol. Microbiol. 47:891-901.
38. Yanofsky MF, Porter SG, Young C, Albright LM, Gordon MP, Nester EW. 1986. The virD operon of Agrobacterium tumefaciens encodes a sitespecific endonuclease. Cell 47:471-477.
39. Atmakuri K, Ding Z, Christie PJ. 2003. VirE2, a type IV secretion substrate, interacts with the VirD4 transfer protein at cell poles of Agrobacterium tumefaciens. Mol. Microbiol. 49:1699-1713.
40. Jakubowski SJ, Krishnamoorthy V, Christie PJ. 2003. Agrobacterium tumefaciens VirB6 protein participates in formation of VirB7 and VirB9 complexes required for type IV secretion. J. Bacteriol. 185:2867-2878.
41. Sagulenko E, Sagulenko V, Chen J, Christie PJ. 2001. Role of Agrobacterium VirB11 ATPase in T-pilus assembly and substrate selection. J. Bacteriol. 183:5813-5825.
42. Zhou X-R, Christie PJ. 1999. Mutagenesis of Agrobacterium VirE2 singlestranded DNA-binding protein identifies regions required for selfassociation and interaction with VirE1 and a permissive site for hybrid protein construction. J. Bacteriol. 181:4342-4352.
43. Atmakuri K, Cascales E, Burton OT, Banta LM, Christie PJ. 2007. Agrobacterium ParA/MinD-like VirC1 spatially coordinates early conjugative DNA transfer reactions. EMBO J. 26:2540-2551.
44. Jakubowski SJ, Cascales E, Krishnamoorthy V, Christie PJ. 2005. Agrobacterium tumefaciens VirB9, an outer-membrane-associated component of a type IV secretion system, regulates substrate selection and T-pilus biogenesis. J. Bacteriol. 187:3486-3495.
45. 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. U. S. A. 102:832-837.
46. van Kregten M, Lindhout BI, Hooykaas PJ, van der Zaal BJ. 2009. Agrobacterium-mediated T-DNA transfer and integration by minimal VirD2 consisting of the relaxase domain and a type IV secretion system translocation signal. Mol. Plant Microbe Interact. 22:1356-1365.
47. Vergunst AC, Schrammeijer B, den Dulk-Ras A, de Vlaam CM, Regensburg-Tuink TJ, Hooykaas PJ. 2000. VirB/D4-dependent protein translocation from Agrobacterium into plant cells. Science 290:979-982.
48. Schrammeijer B, Dulk-Ras Ad A, Vergunst AC, Jurado Jacome E, Hooykaas PJ. 2003. Analysis of Vir protein translocation from Agrobacterium tumefaciens using Saccharomyces cerevisiae as a model: evidence for transport of a novel effector protein VirE3. Nucleic Acids Res. 31:860-868.
49. Shurvinton CE, Hodges L, Ream W. 1992. A nuclear localization signal and the C-terminal omega sequence in the Agrobacterium tumefaciens VirD2 endonuclease are important for tumor formation. Proc. Natl. Acad. Sci. U. S. A. 89:11837-11841.
50. Fullner KJ. 1998. Role of Agrobacterium virB genes in transfer of T complexes and RSF1010. J. Bacteriol. 180:430-434.
51. Das A, Xie YH. 1998. Construction of transposon Tn3phoA: its application in defining the membrane topology of the Agrobacterium tumefaciens DNA transfer proteins. Mol. Microbiol. 27:405-414.
52. Jakubowski SJ, Kerr JE, Garza I, Krishnamoorthy V, Bayliss R, Waksman G, Christie PJ. 2009. Agrobacterium VirB10 domain requirements for type IV secretion and T pilus biogenesis. Mol. Microbiol. 71:779-794.
53. 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. 49:105-116.
54. 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. U. S. A. 100:10465-10470.
55. 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. 182:3705-3716.
56. Merianos HJ, Cadieux N, Lin CH, Kadner RJ, Cafiso DS. 2000. Substrate-induced exposure of an energy-coupling motif of a membrane transporter. Nat. Struct. Biol. 7:205-209.
57. Fanucci GE, Coggshall KA, Cadieux N, Kim M, Kadner RJ, Cafiso DS. 2003. Substrate-induced conformational changes of the periplasmic N terminus of an outer-membrane transporter by site-directed spin labeling. Biochemistry 42:1391-1400.
58. Letoffe S, Delepelaire P, Wandersman C. 1996. Protein secretion in Gram-negative bacteria: assembly of the three components of ABC protein-mediated exporters is ordered and promoted by substrate binding. EMBO J. 15:5804-5811.
59. Thanabalu T, Koronakis E, Hughes C, Koronakis V. 1998. Substrateinduced assembly of a contiguous channel for protein export from E. coli: reversible bridging of an inner-membrane translocase to an outer membrane exit pore. EMBO J. 17:6487-6496.
60. Szpirer CY, Faelen M, Couturier M. 2000. Interaction between the RP4 coupling protein TraG and the pBHR1 mobilization protein Mob. Mol. Microbiol. 37:1283-1292.
61. Thomas J, Hecht DW. 2007. Interaction of Bacteroides fragilis pLV22a relaxase and transfer DNA with Escherichia coli RP4-TraG coupling protein. Mol. Microbiol. 66:948-960.
62. 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. 190:3632-3645.
63. 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. U. S. A. 104:20019-20024.
64. Tato I, Zunzunegui S, de la Cruz F, Cabezon E. 2005. TrwB, the coupling protein involved in DNA transport during bacterial conjugation, is a DNA-dependent ATPase. Proc. Natl. Acad. Sci. U. S. A. 102:8156-8161.
65. 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. 282:25569-22576.
66. Llosa M, Gomis-Ruth FX, Coll M, de la Cruz F. 2002. Bacterial conjugation: a two-step mechanism for DNA transport. Mol. Microbiol. 45: 1-8.
67. 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 151:3505-3516.
68. 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, anintegral protein involved in bacterial conjugation. J. Biol. Chem. 279: 10955-10961.
69. 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 1798:2160-2169.
70. 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 1808:1032-1039.
71. 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 1818:3158-3166.
72. Gomis-Ruth FX, Moncalian G, Perez-Luque R, Gonzalez A, Cabezon E, de la Cruz F, Coll M. 2001. The bacterial conjugation protein TrwB resembles ring helicases and F1-ATPase. Nature 409:637-641.
73. Savvides SN, Yeo HJ, Beck MR, Blaesing F, Lurz R, Lanka E, Buhrdorf R, Fischer W, Haas R, Waksman G. 2003. VirB11 ATPases are dynamic hexameric assemblies: new insights into bacterial type IV secretion. EMBO J. 22:1969-1980.
74. Hare S, Bayliss R, Baron C, Waksman G. 2006. A large domain swap in the VirB11 ATPase of Brucella suis leaves the hexameric assembly intact. J. Mol. Biol. 360:56-66.
75. Savvides SN. 2007. Secretion superfamily ATPases swing big. Structure 15:255-257.
76. Parker C, Meyer RJ. 2007. The R1162 relaxase/primase contains two, type IV transport signals that require the small plasmid protein MobB. Mol. Microbiol. 66:252-261.
77. Kingsman A, Willetts N. 1978. The requirements for conjugalDNAsynthesis in the donor strain during flac transfer. J. Mol. Biol. 122:287-300.
78. 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: 1071-1085.