Membrane insertion stabilizes the structure of TrwB, the R388 conjugative plasmid coupling protein

Biochimica et Biophysica Acta - Biomembranes

Volumn 1808, Issue 4, 2011, Pages 1032-1039

  Vecino, Ana J ^a   De La Arada, Igor ^a,c   Segura, Rosa L ^a   Goñi, Félix M ^a   De La Cruz, Fernando ^b   Arrondo, José L R ^a   Alkorta, Itziar ^a  

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

^b UNIVERSITY OF CANTABRIA   (Spain)

^c GOETHE UNIVERSITY   (Germany)

Author keywords

Bacterial conjugation; Conjugative coupling protein; IR spectroscopy; Membrane protein; Protein reconstitution; R388

Indexed keywords

CARDIOLIPIN; MEMBRANE PROTEIN; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLGLYCEROL; PROTEIN TRWB; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; BACTERIAL MEMBRANE; BACTERIUM CONJUGATION; BETA SHEET; CONTROLLED STUDY; INFRARED SPECTROSCOPY; LIPID ANALYSIS; LIPID BILAYER; MEMBRANE COMPONENT; MICELLE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN DETERMINATION; PROTEIN LIPID INTERACTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; RECOMBINANT PLASMID; STRUCTURE ANALYSIS; THERMOSTABILITY;

DNA-BINDING PROTEINS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; LIPID BILAYERS; LIPOSOMES; MEMBRANE LIPIDS; MEMBRANE PROTEINS; PLASMIDS; PROTEIN DENATURATION; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; TEMPERATURE; TRYPSIN;

BACTERIA (MICROORGANISMS);

EID: 79751525524     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2010.12.025     Document Type: Article

References (49)

1. S. Bolland, M. Llosa, P. Avila, F. de la Cruz, General organization of the conjugal transfer genes of the IncW plasmid R388 and interactions between R388 and IncN and IncP plasmids, J. Bacteriol. 172 (1990) 5795-5802. (Pubitemid 20317117)
2. M. Llosa, S. Bolland, F. de la Cruz, Genetic organization of the conjugal DNA processing region of the IncW plasmid R388, J. Mol. Biol. 235 (1994) 448-464.
3. J.E. Walker, M. Saraste, N.J. Gay, E. coli F1-ATPase interacts with a membrane protein component of a proton channel, Nature 298 (1982) 867-869. (Pubitemid 12046060)
4. I. Hormaeche, I. Alkorta, F. Moro, J.M. Valpuesta, F.M. Goñi, 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)
5. I. Hormaeche, I. Iloro, J.L. Arrondo, F.M. Goñi, F. de la Cruz, 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)
6. I. Hormaeche, R.L. Segura, A.J. Vecino, F.M. Goñi, F. de la Cruz, I. Alkorta, The transmembrane domain provides nucleotide binding specificity to the bacterial conjugation protein TrwB, FEBS Lett. 580 (2006) 3075-3082. (Pubitemid 43729655)
7. A.J. Vecino, R.L. Segura, B. Ugarte-Uribe, S. Águila, F. de la Cruz, F.M. Goñi, I. Alkorta, Reconstitution in liposome bilayers enhances nucleotide binding affinity and ATPspecificity of TrwB conjugative coupling protein, BBA Biomembr. 1798 (11) (2010) 2160-2169.
8. J.L. Arrondo, J. Castresana, J.M. Valpuesta, F.M. Goñi, Structure and thermal denaturation of crystalline and noncrystalline cytochrome oxidase as studied by infrared spectroscopy, Biochemistry 33 (1994) 11650-11655. (Pubitemid 24330100)
9. J.L. Arrondo, F.M. Goñi, Structure and dynamics of membrane proteins as studied by infrared spectroscopy, Prog. Biophys. Mol. Biol. 72 (1999) 367-405.
10. J.L.R. Arrondo, F.M. Goñi, Infrared studies of protein-induced perturbation of lipids in lipoproteins and membranes, Chem. Phys. Lipids 96 (1998) 53-68.
11. I. Tato, S. Zunzunegui, F. de la Cruz, E. Cabezon, TrwB, the coupling protein involved in DNA transport during bacterial conjugation, is a DNA-dependent ATPase, Proc. Natl Acad. Sci. USA 102 (2005) 8156-8161.
12. R.B. Gennis, Biomembranes: molecular structure and function, Springer-Verlag, New York, 1989.
13. M.J. Hope, M.B. Bally, G. Webb, P.R. Cullis, Production of large unilamellar vesicles by a rapid extrusion procedure. Characterization of size distribution, trapped volume and ability to mantain a membrane potential, Biochim. Biophys. Acta 812 (1985) 55-65.
14. D. Lichtenberg, Characterization of the solubilization of lipid bilayers by surfactants, Biochim. Biophys. Acta 821 (1985) 470-478.
15. P.W. Holloway, A simple procedure for removal of Triton X-100 from protein samples, Anal. Biochem. 53 (1973) 304-308.
16. A. Urbani, T. Warne, A colorimetric determination for glycosidic and bile salt-based detergents: applications in membrane protein research, Anal. Biochem. 336 (2005) 117-124.
17. C.S.F. Böttcher, C.M. Van Gent, C. Fries, A rapid and sensitive submicro phosphorus determination, Anal. Chim. Acta 24 (1961) 203-204.
18. J.L. Arrondo, A. Muga, J. Castresana, F.M. Goñi, Quantitative studies of the structure of proteins in solution by Fourier-transform infrared spectroscopy, Prog. Biophys. Mol. Biol. 59 (1993) 23-56.
19. D. Lévy, J.L. Rigaud, Reconstitution of membrane proteins into liposomes, Methods Enzymol. 372 (2003) 65-86. (Pubitemid 37337801)
20. J.L. Rigaud,Membrane proteins: functional and structural studies using reconstituted proteoliposomes and 2-D crystals, Braz. J. Med. Biol. Res. 35 (2002) 753-766.
21. M. Bogdanov, W. Dowhan, Phosphatidylethanolamine is required for in vivo function of the membrane-associated lactose permease of Escherichia coli, J. Biol. Chem. 270 (1995) 732-739.
22. S.H. de Lima, M.L. Lopes, B. Maggio, P. Ciancaglini, Na, K-ATPase reconstituted in liposomes: effects of lipid composition on hydrolytic activity and enzyme orientation, Colloids Surf. B Biointerfaces 41 (2005) 239-248. (Pubitemid 40312740)
23. I. Tato, I. Matilla, I. Arechaga, S. Zunzunegui, F. de la Cruz, 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.
24. M. Garcia-Pacios, J.Á. Fernández-Higuero, I.de laArada, J.L.R. Arrondo, Proteinstability studied by infrared spectroscopy, Biotechnol. Biotechnol. Eq. 22 (2008) 625-628.
25. A. Barth, The infrared absorption of amino acid side chains, Prog. Biophys. Mol. Biol. 74 (2000) 141-173.
26. S.T. Walsh, R.P. Cheng, W.W. Wright, D.O. Alonso, V. Daggett, J.M. Vanderkooi, W.F. DeGrado, The hydration of amides in helices; a comprehensive picture from molecular dynamics, IR, and NMR, Protein Sci. 12 (2003) 520-531.
27. M. Llosa, F.X. Gomis-Ruth, M. Coll, F. de la Cruz, Bacterial conjugation: a two-step mechanism for DNA transport, Mol. Microbiol. 45 (2002) 1-8.
28. F.X. Gomis-Ruth, G. Moncalian, R. Perez-Luque, A. Gonzalez, E. Cabezon, F. de la Cruz, M. Coll, The bacterial conjugation protein TrwB resembles ring helicases and F1-ATPase, Nature 409 (2001) 637-641. (Pubitemid 32154818)
29. E. Goormaghtigh, V. Cabiaux, J. De Meutter, M. Rosseneu, J.M. Ruysschaert, Secondary structure of the particle associating domain of apolipoprotein B-100 in low-density lipoprotein by attenuated total reflection infrared spectroscopy, Biochemistry 32 (1993) 6104-6110. (Pubitemid 23198772)
30. S. Bañuelos, J.L. Arrondo, F.M. Goñi, G. Pifat, Surface-core relationships in human low density lipoprotein as studied by infrared spectroscopy, J. Biol. Chem. 270 (1995) 9192-9196.
31. F. Tanfani, T. Galeazzi, G. Curatola, E. Bertoli, G. Ferretti, Reduced beta-strand content in apoprotein B-100 in smaller and denser low-density lipoprotein subclasses as probed by Fourier-transforminfrared spectroscopy, Biochem. J. 322 (1997) 765-769. (Pubitemid 27135622)
32. J.M. Valpuesta, J.L. Arrondo, M.C. Barbero, M. Pons, F.M. Goñi, Membrane-surfactant interactions. The role of surfactant in mitochondrial complex III-phospholipid-Triton X-100 mixed micelles, J. Biol. Chem. 261 (14) (1986) 6578-6584. (Pubitemid 17204175)
33. T. Haltia, N. Semo, J.L. Arrondo, F.M. Goñi, E. Freire, Thermodynamic and structural stability of cytochrome c oxidase from Paracoccus denitrificans, Biochemistry 33 (1994) 9731-9740. (Pubitemid 24272934)
34. F.X. Gomis-Ruth, G. Moncalian, F. de la Cruz, 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.
35. 2+-ATPase: an infrared study of thermal denaturation and limited proteolysis, Protein Sci. 7 (5) (1998) 1172-1179.
36. I. Iloro, R. Chehín, F.M. Goñi, M.A. Pajares, J.L. Arrondo, Methionine adenosyltransferase alpha-helix structure unfolds at lower temperatures than beta-sheet: a 2D-IR study, Biophys. J. 86 (6) (2004) 3951-3958. (Pubitemid 38780271)
37. J.W. Brauner, C. Dugan, R. Mendelsohn, 13C isotope labelling of hydrophobic peptides. Origin of the anomalous intensity distribution in the infrared amide I spectral region of β-sheet structures, J. Am. Chem. Soc. 122 (4) (2000) 677-683. (Pubitemid 30090505)
38. R. Mendelsohn, H.H. Mantsch, Fourier transform infrared studies of lipid-protein interaction, in: A. Watts, J.J.H.H.M. De Pont (Eds.), Progress in protein-lipid interactions, vol. 2, Elsevier, Amsterdam, 1986, pp. 103-146.
39. J.S. Vrettos, C.W. Meuse, Infrared techniques for quantifying protein structural stability, Anal. Biochem. 390 (2009) 14-20.
40. D. Chapman, J.C. Gómez-Fernández, F.M. Goni, M. Barnard, Difference infrared spectroscopy of aqueous model and biological membranes using an infrared data station, Biochem. Biophys. Methods 2 (6) (1980) 315-323.
41. 2+-ATPase in biomembranes and reconstituted systems, J. Mol. Biol. 157 (4) (1982) 597-618.
42. A. Alonso, C.J. Restall, M. Turner, J.C. Gómez-Fernández, F.M. Goñi, D. Chapman, Protein-lipid interactions and differential scanning calorimetric studies of bacteriorhodopsin reconstituted lipid-water systems, Biochim. Biophys. Acta 689 (2) (1982) 283-289.
43. J.L. Arrondo, M.A. Urbaneja, F.M. Goñi, J.M. Macarulla, G. Sarzala, Protein conformational transitions in sarcoplasmic reticulum membranes, Biochem. Biophys. Res. Commun. 128 (3) (1985) 1159-1163. (Pubitemid 15008267)
44. W.K. Surewicz, M.A. Moscarello, H.H. Mantsch, Secondary structure of the hydrophobic myelin protein in a lipid environment as determined by Fourier-transform infrared spectrometry, J. Biol. Chem. 262 (18) (1987) 8598-8602.
45. J.L. Arrondo, H.H. Mantsch, N. Mullner, S. Pikula, A. Martonosi, Infrared spectroscopic characterization of the structural changes connected with the E1-E2 transition in the Ca2+-ATPase of sarcoplasmic reticulum, J. Biol. Chem. 262 (19) (1987) 9037-9043.
46. R. Mendelsohn, R. Dluhy, T. Taraschi, D.G. Cameron, H.H. Mantsch, Raman and Fourier transform infrared spectroscopic studies of the interaction between glycophorin and dimyristoylphosphatidylcholine, Biochemistry 20 (23) (1981) 6699-6706.
47. G. Anderle, R. Mendelsohn, Fourier-transform infrared studies of CaATPase/phospholipid interaction: survey of lipid classes, Biochemistry 25 (8) (1986) 2174-2179. (Pubitemid 16036033)
48. J.L. Arrondo, F.M. Goñi, J.M. Macarulla, Infrared spectroscopy of phosphatidylcholines in aqueous suspension. A study of the phosphate group vibrations, Biochim. Biophys. Acta 794 (1) (1984) 165-168.
49. F.M. Goñi, J.L. Arrondo, A study of phospholipid phosphate groups in model membranes by Fourier transform infrared spectroscopy, Faraday Discuss. Chem. Soc. 81 (1986) 117-126.