Reconstitution in liposome bilayers enhances nucleotide binding affinity and ATP-specificity of TrwB conjugative coupling protein

Biochimica et Biophysica Acta - Biomembranes

Volumn 1798, Issue 11, 2010, Pages 2160-2169

  Vecino, Ana J ^a   Segura, Rosa L ^a   Ugarte Uribe, Begoña ^a   Águila, Sandra ^a   Hormaeche, Itsaso ^a,c   la Cruz, Fernando de ^b   Goñi, Félix M ^a   Alkorta, Itziar ^a  

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

^b University of Cantabria   (Spain)

^c Progenika Biopharma SA   (Spain)

Author keywords

Bacterial conjugation; Conjugative coupling protein; Membrane protein; Nucleotide binding protein; Protein reconstitution; R388

Indexed keywords

ADENINE NUCLEOTIDE; ADENOSINE TRIPHOSPHATE; GUANINE NUCLEOTIDE; LIPOSOME; MEMBRANE PROTEIN; NUCLEOTIDE; PROTEIN TRWB; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIUM CONJUGATION; BINDING AFFINITY; CONTROLLED STUDY; DELETION MUTANT; ENZYME ACTIVITY; LIPID BILAYER; PRIORITY JOURNAL; PROTEIN DOMAIN;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; CONJUGATION, GENETIC; DNA-BINDING PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FLOW CYTOMETRY; LIPID BILAYERS; NUCLEOTIDES; PROTEOLIPIDS; SUBSTRATE SPECIFICITY;

BACTERIA (MICROORGANISMS);

EID: 79952739479     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2010.07.005     Document Type: Article

References (53)

1. Hormaeche I., Alkorta I., Moro F., Valpuesta J.M., Goñi F.M., de la Cruz F. Purification and properties of TrwB, a hexameric, ATP-binding integral membrane protein essential for R388 plasmid conjugation. J. Biol. Chem. 2002, 277:46456-46462.
2. Cabezón E., Sastre J.I., de la Cruz F. Genetic evidence of a coupling role for the TraG protein family in bacterial conjugation. Mol. Gen. Genet. 1997, 254:400-406.
3. Lin T.S., Kado C.I. The virD4 gene is required for virulence while virD3 and orf5 are not required for virulence of Agrobacterium tumefaciens. Mol. Microbiol. 1993, 9:803-812.
4. 1-ATPase-like molecular motor involved in DNA transport during bacterial conjugation. Res. Microbiol. 2006, 157:299-305.
5. Panicker M.M., Jr E.G. Minkley, purification and properties of the F sex factor TraD protein, an inner membrane conjugal transfer protein. J. Biol. Chem. 1992, 267:12761-12766.
6. Schröder G., Krause S., Zechner E.L., Traxler B., Yeo H.J., Lurz R., Waksman G., Lanka E. TraG-like proteins of DNA transfer systems and of the Helicobacter pylori type IV secretion system: inner membrane gate for exported substrates?. J. Bacteriol. 2002, 184:2767-2779.
7. Hormaeche I., Iloro I., Arrondo J.L., Goñi F.M., de la Cruz F., Alkorta I. Role of the transmembrane domain in the stability of TrwB, an integral protein involved in bacterial conjugation. J. Biol. Chem. 2004, 279:10955-10961.
8. Tato I., Zunzunegui S., de la Cruz F., Cabezon E. TrwB, the coupling protein involved in DNA transport during bacterial conjugation, is a DNA-dependent ATPase. Proc. Natl. Acad. Sci. USA 2005, 102:8156-8161.
9. Hormaeche I., Segura R.L., Vecino A.J., Goñi F.M., de la Cruz F., Alkorta I. The transmembrane domain provides nucleotide binding specificity to the bacterial conjugation protein TrwB. FEBS Lett. 2006, 580:3075-3082.
10. Moncalián G., Cabezon E., Alkorta I., Valle M., Moro F., Valpuesta J.M., Goñi F.M., de la Cruz F. Characterization of ATP and DNA binding activities of TrwB, the coupling protein essential in plasmid R388 conjugation. J. Biol. Chem. 1999, 274:36117-36124.
11. Llosa M., Bolland S., de la Cruz F. Genetic organization of the conjugal DNA processing region of the IncW plasmid R388. J. Mol. Biol. 1994, 235:448-464.
12. Walker J.E., Saraste M., Runswick M.J., Gay N.J. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1982, 1:945-951.
13. 1-ATPase. Nature 2001, 409:637-641.
14. Tato I., Matilla I., Arechaga I., Zunzunegui S., de la Cruz F., Cabezon E. 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. 2007, 282:25569-25576.
15. 2+-ATPase: mechanisms of membrane protein insertion into liposomes during reconstitution procedures involving the use of detergents. Biochim. Biophys. Acta 1992, 1107:283-298.
16. Rigaud J.L., Pitard B., Levy D. Reconstitution of membrane proteins into liposomes: application to energy-transducing membrane proteins. Biochim. Biophys. Acta 1995, 1231:223-246.
17. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
18. Gennis R.B. Biomembranes: Molecular Structure and Function 1989, Springer-Verlag, New York.
19. Hope M.J., Bally M.B., Webb G., Cullis P.R. 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 1985, 812:55-65.
20. Goñi F.M., Alonso A. Spectroscopic techniques in the study of membrane solubilization, reconstitution and permeabilization by detergents. Biochim. Biophys. Acta 2000, 1508:51-68.
21. Lichtenberg D. Characterization of the solubilization of lipid bilayers by surfactants. Biochim. Biophys. Acta 1985, 821:470-478.
22. Holloway P.W. A simple procedure for removal of Triton X-100 from protein samples. Anal. Biochem. 1973, 53:304-308.
23. Urbani A., Warne T. A colorimetric determination for glycosidic and bile salt-based detergents: applications in membrane protein research. Anal. Biochem. 2005, 336:117-124.
24. Bartlett G.R. Phosphorus assay in column chromatography. J. Biol. Chem. 1959, 234:466-468.
25. Böttcher C.S.F., Van Gent C.M., Fries C. A rapid and sensitive submicro phosphorus determination. Anal. Chim. Acta 1961, 24:203-204.
26. Sanowar S., Le Moual H. Functional reconstitution of the Salmonella typhimurium PhoQ histidine kinase sensor in proteoliposomes. Biochem. J. 2005, 390:769-776.
27. Rigaud J.L. Membrane proteins: functional and structural studies using reconstituted proteoliposomes and 2-D crystals. Braz. J. Med. Biol. Res. 2002, 35:753-766.
28. Helenius A., Simons K. Solubilization of membranes by detergents. Biochim. Biophys. Acta 1975, 415:29-79.
29. Rigaud J.L., Paternostre M.T., Bluzat A. Mechanisms of membrane protein insertion into liposomes during reconstitution procedures involving the use of detergents. 2. Incorporation of the light-driven proton pump bacteriorhodopsin. Biochemistry 1988, 27:2677-2688.
30. 1 into liposomes using a new reconstitution procedure. Eur. J. Biochem. 1990, 193:921-925.
31. del Río E., González-Mañas J.M., Gurtubay J.I., Goñi F.M. On the mechanism of bacteriorhodopsin solubilization by surfactants. Arch. Biochem. Biophys. 1991, 291:300-306.
32. Santos H.L., Lamas R.P., Ciancaglini P. Solubilization of Na, K-ATPase from rabbit kidney outer medulla using only C12E8. Braz. J. Med. Biol. Res. 2002, 35:277-288.
33. 2+-ATPase from bovine pulmonary artery smooth muscle microsomes by different detergents: preservation of native structure and function of the enzyme by DHPC. Biochim. Biophys. Acta 2006, 1760:20-31.
34. Lévy D., Rigaud J.L. Reconstitution of membrane proteins into liposomes. Methods Enzymol. 2003, 372:65-86.
35. Lévy D., Bluzat A., Seigneuret M., Rigaud J.L. A systematic study of liposome and proteoliposome reconstitution involving Bio-Bead-mediated Triton X-100 removal. Biochim. Biophys. Acta 1990, 1025:179-190.
36. Daghastanli K.R., Ferreira R.B., Jr G., Thedei B.Maggio, Ciancaglini P. Lipid composition-dependent incorporation of multiple membrane proteins into liposomes. Colloids Surf. B Biointerfaces 2004, 36:127-137.
37. 2+)ATPase reconstituted with synthetic phospholipids. FEBS Lett. 1979, 98:224-228.
38. Alonso A., Restall C.J., Turner M., Gomez-Fernandez J.C., Goñi F.M., Chapman D. Protein-lipid interactions and differential scanning calorimetric studies of bacteriorhodopsin reconstituted lipid-water systems. Biochim. Biophys. Acta 1982, 689:283-289.
39. Hiratsuka T., Uchida K. Preparation and properties of 2'(or 3')-O-(2, 4, 6-trinitrophenyl) adenosine 5'-triphosphate, an analogue of adenosine triphosphate. Biochim. Biophys. Acta 1973, 320:635-647.
40. Cheng Y., Prusoff W.H. Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic reaction. Biochem. Pharmacol. 1973, 22:3099-3108.
41. Groth G., Walker E. ATP synthase from bovine heart mitochondria: reconstitution into unilamellar phospholipid vesicles of the pure enzyme in a functional state. Biochem. J. 1996, 318:351-357.
42. Cladera J., Rigaud J.L., Villaverde J., Duñach M. Liposome solubilization and membrane protein reconstitution using Chaps and Chapso. Eur. Biochem. 1997, 243:798-804.
43. Velamakanni S., Yao Y., Gutmann D.A., van Veen H.W. Multidrug transport by the ABC transporter Sav1866 from Staphylococcus aureus. Biochemistry 2008, 47:9300-9308.
44. Zehnpfennig B., Urbatsch I.L., Galla H.J. Functional reconstitution of human ABCC3 into proteoliposomes reveals a transport mechanism with positive cooperativity. Biochemistry 2009, 48:4423-4430.
45. Devesa F., Chams V., Dinadayala P., Stella A., Ragas A., Auboiroux H., Stegmann T., Poquet Y. Functional reconstitution of the HIV receptors CCR5 and CD4 in liposomes. Eur. J. Biochem. 2002, 269:5163-5174.
46. Sahu S.K., Gummadi S.N. Flippase activity in proteoliposomes reconstituted with Spinacea oleracea endoplasmic reticulum membrane proteins: evidence of biogenic membrane flippase in plants. Biochemistry 2008, 47:10481-10490.
47. MirAfzali Z., Leipprandt J.R., McCracken J.L., DeWitt D.L. Fast efficient reconstitution of the cyclooxygenases into proteoliposomes. Arch. Biochem. Biophys. 2005, 443:60-65.
48. de Lima S.H., Lopes M.L., Maggio B., Ciancaglini P. Na, K-ATPase reconstituted in liposomes: effects of lipid composition on hydrolytic activity and enzyme orientation. Colloids Surf. B Biointerfaces 2005, 41:239-248.
49. Dröse S., Galkin A., Brandt U. Proton pumping by complex I (NADH:ubiquinone oxidoreductase) from Yarrowia lipolytica reconstituted into proteoliposomes. Biochim. Biophys. Acta 2005, 1710:87-95.
50. Llosa M., Zunzunegui S., de la Cruz F. Conjugative coupling proteins interact with cognate and heterologous VirB10-like proteins while exhibiting specificity for cognate relaxosomes. Proc. Natl. Acad. Sci. USA 2003, 100:10465-10470.
51. Schröder G., Lanka E. The mating pair formation system of conjugative plasmids-a versatile secretion machinery for transfer of proteins and DNA. Plasmid 2005, 54:1-25.
52. Niu S.L., Doctrow B., Mitchell D.C. Rhodopsin activity varies in proteoliposomes prepared by different techniques. Biochemistry 2009, 48:156-163.
53. Tikhonova E.B., Devroy V.K., Lau S.Y., Zgurskaya H.I. Reconstitution of the Escherichia coli macrolide transporter: the periplasmic membrane fusion protein MacA stimulates the ATPase activity of MacB. Mol. Microbiol. 2007, 63:895-910.