The membrane bound bacterial lipocalin Blc is a functional dimer with binding preference for lysophospholipids

FEBS Letters

Volumn 580, Issue 20, 2006, Pages 4877-4883

  Campanacci, Valérie ^a   Bishop, Russell E ^b   Blangy, Stéphanie ^a   Tegoni, Mariella ^a   Cambillau, Christian ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

Blc; Crystal structure; Fatty acids; Lipocalins; Lysophospholipids

Indexed keywords

BACTERIAL PROTEIN; BLC PROTEIN; DIMER; FATTY ACID; LIPOCALIN; LYSOPHOSPHOLIPID; MEMBRANE PROTEIN; PHOSPHOLIPID; UNCLASSIFIED DRUG; VACCENIC ACID;

ARTICLE; BACTERIAL MEMBRANE; BINDING SITE; CRYSTAL STRUCTURE; FLUORESCENCE; HYPOTHESIS; LIPID METABOLISM; NONHUMAN; PHOTOCHEMICAL QUENCHING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION;

AMINO ACID SEQUENCE; BACTERIAL OUTER MEMBRANE PROTEINS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FATTY ACIDS; LIPOPROTEINS; LYSOPHOSPHOLIPIDS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; OLEIC ACIDS; PROTEIN STRUCTURE, QUATERNARY; SEQUENCE ALIGNMENT;

BACTERIA (MICROORGANISMS); EUKARYOTA; NEGIBACTERIA;

EID: 33748629117     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2006.07.086     Document Type: Article

References (50)

1. Flower D.R., North A.C., and Sansom C.E. The lipocalin protein family: structural and sequence overview. Biochim. Biophys. Acta 1482 (2000) 9-24
2. Bishop R.E., Penfold S.S., Frost L.S., Holtje J.V., and Weiner J.H. Stationary phase expression of a novel Escherichia coli outer membrane lipoprotein and its relationship with mammalian apolipoprotein D. Implications for the origin of lipocalins. J. Biol. Chem. 270 (1995) 23097-23103
3. Bishop R.E. The bacterial lipocalins. Biochim. Biophys. Acta 1482 (2000) 73-83
4. Akerstrom B., Flower D.R., and Salier J.P. Lipocalins: unity in diversity. Biochim. Biophys. Acta 1482 (2000) 1-8
5. Newcomer M.E., Jones T.A., Aqvist J., Sundelin J., Eriksson U., Rask L., and Peterson P.A. The three-dimensional structure of retinol-binding protein. Embo J. 3 (1984) 1451-1454
6. Flower D.R. Experimentally determined lipocalin structures. Biochim. Biophys. Acta 1482 (2000) 46-56
7. Ramoni R., Vincent F., Grolli S., Conti V., Malosse C., Boyer F.D., Nagnan-Le Meillour P., Spinelli S., Cambillau C., and Tegoni M. The insect attractant 1-octen-3-ol is the natural ligand of bovine odorant-binding protein. J. Biol. Chem. 276 (2001) 7150-7155
8. Spinelli S., Ramoni R., Grolli S., Bonicel J., Cambillau C., and Tegoni M. The structure of the monomeric porcine odorant binding protein sheds light on the domain swapping mechanism. Biochemistry 37 (1998) 7913-7918
9. Ramoni R., Vincent F., Ashcroft A.E., Accornero P., Grolli S., Valencia C., Tegoni M., and Cambillau C. Control of domain swapping in bovine odorant-binding protein. Biochem J. 365 (2002) 739-748
10. Gutierrez G., Ganfornina M.D., and Sanchez D. Evolution of the lipocalin family as inferred from a protein sequence phylogeny. Biochim. Biophys. Acta 1482 (2000) 35-45
11. Campanacci V., Nurizzo D., Spinelli S., Valencia C., Tegoni M., and Cambillau C. The crystal structure of the Escherichia coli lipocalin Blc suggests a possible role in phospholipid binding. FEBS Lett. 562 (2004) 183-188
12. Huber R., Schneider M., Mayr I., Muller R., Deutzmann R., Suter F., Zuber H., Falk H., and Kayser H. Molecular structure of the bilin binding protein (BBP) from Pieris brassicae after refinement at 2.0 A resolution. J. Mol. Biol. 198 (1987) 499-513
13. Snijder H.J., Ubarretxena-Belandia I., Blaauw M., Kalk K.H., Verheij H.M., Egmond M.R., Dekker N., and Dijkstra B.W. Structural evidence for dimerization-regulated activation of an integral membrane phospholipase. Nature 401 (1999) 717-721
14. Ahn V.E., Lo E.I., Engel C.K., Chen L., Hwang P.M., Kay L.E., Bishop R.E., and Prive G.G. A hydrocarbon ruler measures palmitate in the enzymatic acylation of endotoxin. Embo J. 23 (2004) 2931-2941
15. Ganfornina M.D., Sanchez D., and Bastiani M.J. Lazarillo, a new GPI-linked surface lipocalin, is restricted to a subset of neurons in the grasshopper embryo. Development 121 (1995) 123-134
16. Davis R.a.V.J.E. Comprehensive Biochemistry (1996), Elsevier, Amsterdam
17. Breustedt D.A., Schonfeld D.L., and Skerra A. Comparative ligand-binding analysis of ten human lipocalins. Biochim. Biophys. Acta 1764 (2006) 161-173
18. Vincentelli R., Bignon C., Gruez A., Canaan S., Sulzenbacher G., Tegoni M., Campanacci V., and Cambillau C. Medium-scale structural genomics: strategies for protein expression and crystallization. Acc. Chem. Res. 36 (2003) 165-172
19. Campanacci V., Krieger J., Bette S., Sturgis J.N., Lartigue A., Cambillau C., Breer H., and Tegoni M. Revisiting the specificity of Mamestra brassicae and Antheraea polyphemus pheromone-binding proteins with a fluorescence binding assay. J. Biol. Chem. 276 (2001) 20078-20084
20. Sulzenbacher G., Gruez A., Roig-Zamboni V., Spinelli S., Valencia C., Pagot F., Vincentelli R., Bignon C., Salomoni A., Grisel S., Maurin D., Huyghe C., Johansson K., Grassick A., Roussel A., Bourne Y., Perrier S., Miallau L., Cantau P., Blanc E., Genevois M., Grossi A., Zenatti A., Campanacci V., and Cambillau C. A medium-throughput crystallization approach. Acta Crystallogr. D Biol. Crystallogr. 58 (2002) 2109-2115
21. CCP4 & 4, C.C.P.N. The CCP4 suite: programs for crystallography, Acta Cryst D. 50, 1994, 760-766.
22. Murshudov G., Vagin A.A., and Dodson EJ. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D 53 (1997) 240-255
23. Roussel, A. & Cambillau, C. (1991). The TURBO-FRODO graphics package., Silicon graphics Geometry Partners Directory, Mountain View, USA.
24. DeLano, W. The PyMOL Molecular Graphics System (http://www.pymol.org), DeLano Scientific LLC, San Carlos, CA, USA.
25. Vincent F., Ramoni R., Spinelli S., Grolli S., Tegoni M., and Cambillau C. Crystal structures of bovine odorant-binding protein in complex with odorant molecules. Eur. J. Biochem. 271 (2004) 3832-3842
26. Briand L., Nespoulous C., Perez V., Remy J.J., Huet J.C., and Pernollet J.C. Ligand-binding properties and structural characterization of a novel rat odorant-binding protein variant. Eur. J. Biochem. 267 (2000) 3079-3089
27. Marchese S., Pes D., Scaloni A., Carbone V., and Pelosi P. Lipocalins of boar salivary glands binding odours and pheromones. Eur. J. Biochem. 252 (1998) 563-568
28. Miller S., Lesk A.M., Janin J., and Chothia C. The accessible surface area and stability of oligomeric proteins. Nature 328 (1987) 834-836
29. Desmyter A., Spinelli S., Payan F., Lauwereys M., Wyns L., Muyldermans S., and Cambillau C. Three camelid VHH domains in complex with porcine pancreatic alpha-amylase. Inhibition and versatility of binding topology. J. Biol. Chem. 277 (2002) 23645-23650
30. Walhout A.J., Temple G.F., Brasch M.A., Hartley J.L., Lorson M.A., van den Heuvel S., and Vidal M. GATEWAY recombinational cloning: application to the cloning of large numbers of open reading frames or ORFeomes. Methods Enzymol. 328 (2000) 575-592
31. Tegoni M., Ramoni R., Bignetti E., Spinelli S., and Cambillau C. Domain swapping creates a third putative combining site in bovine odorant binding protein dimer. Nat. Struct. Biol. 3 (1996) 863-867
32. Doerrler W.T., Gibbons H.S., and Raetz C.R. MsbA-dependent translocation of lipids across the inner membrane of Escherichia coli. J. Biol. Chem. 279 (2004) 45102-45109
33. Reyes C.L., and Chang G. Structure of the ABC transporter MsbA in complex with ADP. vanadate and lipopolysaccharide. Science 308 (2005) 1028-1031
34. Bos M.P., Tefsen B., Geurtsen J., and Tommassen J. Identification of an outer membrane protein required for the transport of lipopolysaccharide to the bacterial cell surface. Proc. Natl. Acad. Sci. USA 101 (2004) 9417-9422
35. Dirusso C.C., and Black P.N. Bacterial long chain fatty acid transport: gateway to a fatty acid-responsive signaling system. J. Biol. Chem. 279 (2004) 49563-49566
36. Jones N.C., and Osborn M.J. Interaction of Salmonella typhimurium with phospholipid vesicles. Incorporation of exogenous lipids into intact cells. J. Biol. Chem. 252 (1977) 7398-7404
37. Jones N.C., and Osborn M.J. Translocation of phospholipids between the outer and inner membranes of Salmonella typhimurium. J. Biol. Chem. 252 (1977) 7405-7412
38. Huijbregts R.P., de Kroon A.I., and de Kruijff B. Topology and transport of membrane lipids in bacteria. Biochim. Biophys. Acta 1469 (2000) 43-61
39. Tokuda H., and Matsuyama S. Sorting of lipoproteins to the outer membrane in E. coli. Biochim. Biophys. Acta 1693 (2004) 5-13
40. Hsu L., Jackowski S., and Rock C.O. Uptake and acylation of 2-acyl-lysophospholipids by Escherichia coli. J. Bacteriol. 171 (1989) 1203-1205
41. Hsu L., Jackowski S., and Rock C.O. Isolation and characterization of Escherichia coli K-12 mutants lacking both 2-acyl-glycerophosphoethanolamine acyltransferase and acyl-acyl carrier protein synthetase activity. J. Biol. Chem. 266 (1991) 13783-13788
42. Bishop R.E., Gibbons H.S., Guina T., Trent M.S., Miller S.I., and Raetz C.R. Transfer of palmitate from phospholipids to lipid A in outer membranes of gram-negative bacteria. Embo J. 19 (2000) 5071-5080
43. Hwang P.M., Choy W.Y., Lo E.I., Chen L., Forman-Kay J.D., Raetz C.R., Prive G.G., Bishop R.E., and Kay L.E. Solution structure and dynamics of the outer membrane enzyme PagP by NMR. Proc. Natl. Acad. Sci. USA 99 (2002) 13560-13565
44. Hwang P.M., Bishop R.E., and Kay L.E. The integral membrane enzyme PagP alternates between two dynamically distinct states. Proc. Natl. Acad. Sci. USA 101 (2004) 9618-9623
45. Jia W., Zoeiby A.E., Petruzziello T.N., Jayabalasingham B., Seyedirashti S., and Bishop R.E. Lipid trafficking controls endotoxin acylation in outer membranes of Escherichia coli. J. Biol. Chem. 279 (2004) 44966-44975
46. Pluckthun A., and Dennis E.A. Acyl and phosphoryl migration in lysophospholipids: importance in phospholipid synthesis and phospholipase specificity. Biochemistry 21 (1982) 1743-1750
47. Anliker B., and Chun J. Lysophospholipid G protein-coupled receptors. J. Biol. Chem. 279 (2004) 20555-20558
48. Morais Cabral J.H., Atkins G.L., Sanchez L.M., Lopez-Boado Y.S., Lopez-Otin C., and Sawyer L. Arachidonic acid binds to apolipoprotein D: implications for the protein's function. FEBS Lett. 366 (1995) 53-56
49. Walker D.W., Muffat J., Rundel C., and Benzer S. Overexpression of a Drosophila homolog of apolipoprotein d leads to increased stress resistance and extended lifespan. Curr. Biol. 16 (2006) 674-679
50. Sanchez D., Lopez-Arias B., Torroja L., Canal I., Wang X., Bastiani M.J., and Ganfornina M.D. Loss of glial lazarillo, a homolog of apolipoprotein d, reduces lifespan and stress resistance in Drosophila. Curr. Biol. 16 (2006) 680-686