Monomer-to-dimer transition of Brucella suis type IV secretion system component VirB8 induces conformational changes

FEBS Journal

Volumn 284, Issue 8, 2017, Pages 1218-1232

  Sharifahmadian, Mahzad ^a   Arya, Tarun ^a   Bessette, Benoit ^a   Lecoq, Lauriane ^a   Ruediger, Edward ^b   Omichinski, James G ^a   Baron, Christian ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

Author keywords

antibiotic resistance; crystal structure; NMR assignment; type IV secretion system; VirB8

Indexed keywords

3 [(3 CHOLAMIDOPROPYL)DIMETHYLAMMONIO] 1 PROPANESULFONIC ACID; AMIDE; DIMER; INTRINSICALLY DISORDERED PROTEIN; MONOMER; PROTEIN VARIANT; UNCLASSIFIED DRUG; VIRB8 PROTEIN; VIRULENCE FACTOR; BACTERIAL PROTEIN; MICELLE; TYPE IV SECRETION SYSTEM;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; BETA SHEET; BINDING AFFINITY; BRUCELLA SUIS; CONCENTRATION (PARAMETERS); CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIFFERENTIAL SCANNING FLUORIMETRY; DIMERIZATION; FLUOROMETRY; MICELLE; MOLECULAR DOCKING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PERIPLASM; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTON NUCLEAR MAGNETIC RESONANCE; SIZE EXCLUSION CHROMATOGRAPHY; TYPE IV SECRETION SYSTEM; WILD TYPE; X RAY CRYSTALLOGRAPHY; CHEMISTRY; METABOLISM; NUCLEAR MAGNETIC RESONANCE; PROTEIN CONFORMATION;

BACTERIAL PROTEINS; BRUCELLA SUIS; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; FLUOROMETRY; MICELLES; MOLECULAR DOCKING SIMULATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PERIPLASM; PROTEIN CONFORMATION; TYPE IV SECRETION SYSTEMS;

EID: 85016443143     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.14049     Document Type: Article

References (53)

1. Fronzes R, Christie PJ & Waksman G (2009) The structural biology of type IV secretion systems. Nat Rev Microbiol 7, 703–714.
2. Trokter M, Felisberto-Rodrigues C, Christie PJ & Waksman G (2014) Recent advances in the structural and molecular biology of type IV secretion systems. Curr Opin Struct Biol 27C, 16–23.
3. Chandran Darbari V & Waksman G (2015) Structural biology of bacterial type IV secretion systems. Annu Rev Biochem 84, 603–629.
4. Goessweiner-Mohr N, Arends K, Keller W & Grohmann E (2013) Conjugative type IV secretion systems in Gram-positive bacteria. Plasmid 70, 289–302.
5. Lai E-M & Kado CI (1998) Processed VirB2 is the major subunit of the promiscuous pilus of Agrobacterium tumefaciens. J Bacteriol 180, 2711–2717.
6. Eisenbrandt R, Kalkum M, Lai EM, Lurz R, Kado CI & Lanka E (1999) Conjugative pili of IncP plasmids, and the Ti plasmid T pilus are composed of cyclic subunits. J Biol Chem 274, 22548–22555.
7. Aly KA & Baron C (2007) The VirB5 protein localizes to the T-pilus tips in Agrobacterium tumefaciens. Microbiology 153, 3766–3775.
8. Kwok T, Zabler D, Urman S, Rohde M, Hartig R, Wessler S, Misselwitz R, Berger J, Sewald N, Konig W et al. (2007) Helicobacter exploits integrin for type IV secretion and kinase activation. Nature 449, 862–866.
9. Thorstenson YR & Zambryski PC (1994) The essential virulence protein VirB8 localizes to the inner membrane of Agrobacterium tumefaciens. J Bacteriol 176, 1711–1717.
10. Buhrdorf R, Forster C, Haas R & Fischer W (2003) Topological analysis of a putative VirB8 homologue essential for the cag type IV secretion system in Helicobacter pylori. Int J Med Microbiol 293, 213–217.
11. O'Callaghan D, Cazevieille C, Allardet-Servent A, Boschiroli ML, Bourg G, Foulongne V, Frutos P, Kulakov Y & Ramuz M (1999) A homologue of the Agrobacterium tumefaciens VirB and Bordetella pertussis Ptl type IV secretion systems is essential for intracellular survival of Brucella suis. Mol Microbiol 33, 1210–1220.
12. Fercher C, Probst I, Kohler V, Goessweiner-Mohr N, Arends K, Grohmann E, Zangger K, Meyer NH & Keller W (2016) VirB8-like protein TraH is crucial for DNA transfer in Enterococcus faecalis. Sci Rep 6, 24643.
13. Das A & Xie Y-H (2000) The Agrobacterium T-DNA transport pore proteins VirB8, VirB9 and VirB10 interact with one another. J Bacteriol 182, 758–763.
14. Yuan Q, Carle A, Gao C, Sivanesan D, Aly K, Höppner C, Krall L, Domke N & Baron C (2005) Identification of the VirB4-VirB8-VirB5-VirB2 pilus assembly sequence of type IV secretion systems. J Biol Chem 280, 26349–26359.
15. Paschos A, Patey G, Sivanesan D, Gao C, Bayliss R, Waksman G, O'Callaghan D & Baron C (2006) Dimerization and interactions of Brucella suis VirB8 with VirB4 and VirB10 are required for its biological activity. Proc Natl Acad Sci USA 103, 7252–7257.
16. Bourg G, Sube R, O'Callaghan D & Patey G (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, 2985–2992.
17. Sivanesan D, Hancock MA, Villamil Giraldo AM & Baron C (2010) Quantitative analysis of VirB8-VirB9-VirB10 interactions provides a dynamic model of type IV secretion system core complex assembly. Biochemistry 49, 4483–4493.
18. Villamil Giraldo AM, Sivanesan D, Carle A, Paschos A, Smith MA, Plesa M, Coulton J & Baron C (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, 3881–3890.
19. Casu B, Smart JP, 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, 23817–23829.
20. Terradot L, Bayliss R, Oomen C, Leonard G, Baron C & Waksman G (2005) Crystal Structures of the periplasmic domains 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 102, 4596–4601.
21. Bailey S, Ward D, Middleton R, Grossmann JG & Zambryski P (2006) Agrobacterium tumefaciens VirB8 structure reveals potential protein-protein interactions sites. Proc Natl Acad Sci USA 103, 2582–2587.
22. Porter CJ, Bantwal R, Bannam TL, Rosado CJ, Pearce MC, Adams V, Lyras D, Whisstock JC & Rood JI (2012) 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, 275–288.
23. Goessweiner-Mohr N, Grumet L, Arends K, Pavkov-Keller T, Gruber CC, Gruber K, Birner-Gruenberger R, Kropec-Huebner A, Huebner J, Grohmann E et al. (2013) The 2.5 Å structure of the Enterococcus conjugation protein TraM resembles VirB8 type IV secretion proteins. J Biol Chem 288, 2018–2028.
24. Sivanesan D & Baron C (2011) The dimer interface of Agrobacterium tumefaciens VirB8 is important for type IV secretion system function, stability and for association of VirB2 with the core complex. J Bacteriol 193, 2097–2106.
25. Smith MA, Coincon M, Paschos A, Jolicoeur B, Lavallee P, Sygusch J & Baron C (2012) Identification of the binding site of brucella VirB8 interaction inhibitors. Chem Biol 19, 1041–1048.
26. Paschos A, den Hartigh A, Smith MA, Atluri VL, Sivanesan D, Tsolis RM & Baron C (2011) An in vivo high-throughput screening approach targeting the type IV secretion system component VirB8 identified inhibitors of Brucella abortus 2308 proliferation. Infect Immun 79, 1033–1043.
27. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J & Bax A (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6, 277–293.
28. Gillespie JJ, Phan IQ, Scheib H, Subramanian S, Edwards TE, Lehman SS, Piitulainen H, Rahman MS, Rennoll-Bankert KE, Staker BL et al. (2015) Structural insight into how bacteria prevent interference between multiple divergent type IV secretion systems. mBio 6, e01867–15.
29. Vranken WF, Boucher W, Stevens TJ, Fogh RH, Pajon A, Llinas M, Ulrich EL, Markley JL, Ionides J & Laue ED (2005) The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins 59, 687–696.
30. Bodenhausen G & Ruben DJ (1980) Natural abundance nitrogen-15 NMR by enhanced heteronuclear spectroscopy. Chem Phys Lett 69, 185–189.
31. Bax A & Ikura M (1991) An efficient 3D NMR technique for correlating the proton and 15N backbone amide resonances with the alpha-carbon of the preceding residue in uniformly 15N/13C enriched proteins. J Biomol NMR 1, 99–104.
32. Wittekind M & Mueller L (1993) HNCACB, a high-sensitivity 3D NMR experiment to correlate amide-proton and nitrogen resonances with the alpha- and beta-carbon resonances in proteins. J Magn Reson B 101, 201–205.
33. Kay LE, Xu GY & Yamazaki T (1994) Enhanced-sensitivity triple-resonance spectroscopy with minimal H2O saturation. J Magn Reson A 109, 129–133.
34. Clubb RT, Venkataraman T & Wagner G (1969) A constant-time three-dimensional triple-resonance pulse scheme to correlate intraresidue 1HN, 15N, and 13C’ chemical shifts in 15N-13C-labelled proteins. J Magn Reson 97, 213–217.
35. Grzesiek S & Bax A (1992) Correlating backbone amide and side-chain resonances in larger proteins by multiple relayed triple resonance NMR. J Am Chem Soc 114, 6291–6293.
36. Pascal SM, Muhandiram DR, Yamazaki T, Forman-Kay JD & Kay LE (1994) Simultaneous acquisition of 15N- and 13C-edited NOE spectra of proteins dissolved in H2O. J Magn Reson A 103, 197–201.
37. Schwarzinger S, Kroon GJA, Foss TR, Chung J, Wright PE & Dyson HJ (2001) Sequence-dependent correlation of random coil NMR chemical shifts. J Am Chem Soc 123, 2970–2978.
38. Wishart DS & Sykes BD (1994) The 13C chemical-shift index: a simple method for the identification of protein secondary structure using 13C chemical-shift data. J Biomol NMR 4, 171–180.
39. Wishart DS, Sykes BD & Richards FM (1992) The chemical shift index: a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy. Biochemistry 31, 1647–1651.
40. Congreve M, Carr R, Murray C & Jhoti H (2003) A ‘rule of three’ for fragment-based lead discovery? Drug Discovery Today 8, 876–877.
41. Otwinowski Z & Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276, 307–326.
42. Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, Moriarty NW, Read RJ, Sacchettini JC, Sauter NK & Terwilliger TC (2002) PHENIX: building new software for automated crystallographic structure determination, Acta crystallographica. Acta Crystallogr D Biol Crystallogr 58, 1948–1954.
43. Murshudov GN, Vagin AA & Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method, Acta crystallographica. Acta Crystallogr D Biol Crystallogr 53, 240–255.
44. Emsley P & Cowtan K (2004) Coot: model-building tools for molecular graphics, Acta crystallographica. Acta Crystallogr D Biol Crystallogr 60, 2126–2132.
45. DeLano WL (2002) The PyMOL Molecular Graphics System. DeLano Scientific LLC, San Carlos, CA, USA.
46. Morris GM, Goodsell DS, Halliday RS, Huey R, Hart WE, Belew RK & Olson AJ (1998) Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. J Comput Chem 19, 1639–1662.
47. Morris GM, Huey R & Olson AJ (2008) Using autodock for ligand-receptor docking. Curr Protoc Bioinformatics 14, 8–14.
48. Irwin JJ, Sterling T, Mysinger MM, Bolstad ES & Coleman RG (2012) ZINC: a free tool to discover chemistry for biology. J Chem Inf Model 52, 1757–1768.
49. Mashalidis EH, Sledz P, Lang S & Abell C (2013) A three-stage biophysical screening cascade for fragment-based drug discovery. Nat Protoc 8, 2309–2324.
50. Lee IY, Gruber TD, Samuels A, Yun M, Nam B, Kang M, Crowley K, Winterroth B, Boshoff HI & Barry CE 3rd (2013) Structure-activity relationships of antitubercular salicylanilides consistent with disruption of the proton gradient via proton shuttling. Bioorg Med Chem 21, 114–126.
51. Gong Y, Somersan Karakaya S, Guo X, Zheng P, Gold B, Ma Y, Little D, Roberts J, Warrier T, Jiang X et al. (2014) Benzimidazole-based compounds kill Mycobacterium tuberculosis. Eur J Med Chem 75, 336–353.
52. Goudreau N, Lemke CT, Faucher AM, Grand-Maitre C, Goulet S, Lacoste JE, Rancourt J, Malenfant E, Mercier JF, Titolo S et al. (2013) Novel inhibitor binding site discovery on HIV-1 capsid N-terminal domain by NMR and X-ray crystallography. ACS Chem Biol 8, 1074–1082.
53. Yanisch-Perron C, Viera J & Messing J (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequence of the M13mp18 and pUC18 vectors. Gene 33, 103–119.