Brucella abortus MFP: A trimeric coiled-coil protein with membrane fusogenic activity

Biochemistry

Volumn 47, Issue 31, 2008, Pages 8165-8175

  Carrica, Mariela Del Carmen ^a   Craig, Patricio Oliver ^b   Alonso, Silvia Del Valle ^c   Goldbaum, Fernando Alberto ^b   Cravero, Silvio Lorenzo ^a  

^a INSTITUTO NACIONAL DE TECNOLOGÍA AGROPECUARIA INTA   (Argentina)

^b FUNDACIÓN INSTITUTO LELOIR   (Argentina)

^c UNIVERSIDAD NACIONAL DE QUILMES   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

AMINES; HEALTH; IONIC STRENGTH; LIPOSOMES; PHOSPHOLIPIDS; PORT TERMINALS; PROTEINS; SOAPS (DETERGENTS);

ACIDIC PH; AMINO-TERMINAL DOMAIN; AMPHIPATHIC; BACTERIAL GENUS; BIOCHEMICAL CHARACTERIZATIONS; BRUCELLA; CARBOXYL-TERMINAL; COILED-COIL DOMAINS; FUNCTIONAL PROPERTIES; HELICAL STRUCTURES; IN-VITRO; INTRACELLULAR PATHOGENS; MEMBRANE FUSION; PHOSPHOLIPID VESICLES; PROTEOBACTERIA; STRUCTURAL DOMAINS; STRUCTURAL REARRANGEMENTS;

CELL MEMBRANES;

DETERGENT; PHOSPHOLIPID; PROTEIN;

ACIDITY; ALPHA HELIX; ARTICLE; BIOCHEMISTRY; BRUCELLA ABORTUS; CARBOXY TERMINAL SEQUENCE; IN VITRO STUDY; IONIC STRENGTH; MEMBRANE FUSION; NONHUMAN; PHOSPHOLIPID VESICLE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOBACTERIA; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BRUCELLA ABORTUS; CIRCULAR DICHROISM; DIMERIZATION; LIPOSOMES; MEMBRANE FUSION; MEMBRANE LIPIDS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; PHOSPHOLIPIDS; POLYMERASE CHAIN REACTION; PROTEIN BINDING; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROMETRY, FLUORESCENCE;

ANIMALIA; BACTERIA (MICROORGANISMS); BRUCELLA; BRUCELLA MELITENSIS BIOVAR ABORTUS; PROTEOBACTERIA;

EID: 48649084513     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi800462y     Document Type: Article

References (52)

1. Corbel, M. J. (1997) Brucellosis: An overview. Emerging Infect. Dis. 3, 213-221.
2. DelVecchio, V. G., Kapatral, V., Redkar, R. J., Patra, G., Mujer, C., Los, T., Ivanova, N., Anderson, I., Bhattacharyya, A., Lykidis, A., Reznik, G., Jablonski, L., Larsen, N., D'Souza, M., Bernal, A., Mazur, M., Goltsman, E., Selkov, E., Elzer, P. H., Hagius, S., O'Callaghan, D., Letesson, J. J., Haselkorn, R., Kyrpides, N., and Overbeek, R. (2002) The genome sequence of the facultative intracellular pathogen Brucella melitensis. Proc. Natl. Acad. Sci. U.S.A. 99, 443-448.
3. Jones, S. M., and Winter, A. J. (1992) Survival of virulent and attenuated strains of Brucella abortus in normal and gamma interferon-activated murine peritoneal macrophages. Infect. Immun. 60, 3011-3014.
4. Detilleux, P. G., Deyoe, B. L., and Cheville, N. F. (1990) Penetration and intracellular growth of Brucella abortus in non-phagocytic cells in vitro. Infect. Immun. 58, 2320-2328.
5. Gorvel, J. P., and Moreno, E. (2002) Brucella intracellular life: From invasion to intracellular replication. Vet. Microbiol. 90, 281-297.
6. Roop, R. M., II, Bellaire, B. H., Valderas, M. W., and Cardelli, J. A. (2004) Adaptation of the Brucellae to their intracellular niche. Mol. Microbiol. 52, 621-630.
7. Porte, F., Liautard, J. P., and Kohler, S. (1999) Early acidification of phagosomes containing Brucella suis is essential for intracellular survival in murine macrophages. Infect. Immun. 67, 4041-4047.
8. Lopez-Goni, I., Guzman-Verri, C., Manterola, L., Sola-Landa, A., Moriyon, I., and Moreno, E. (2002) Regulation of Brucella virulence by the two-component system BvrR/BvrS. Vet. Microbiol. 90, 329-339.
9. Boschiroli, M. L., Ouahrani-Bettache, S., Foulongne, V., Michaux-Charachon, S., Bourg, G., Allardet-Servent, A., Cazevieille, C., Lavigne, J. P., Liautard, J. P., Ramuz, M., and O'Callaghan, D. (2002) Type IV secretion and Brucella virulence. Vet. Microbiol. 90, 341-348.
10. Roop, R. M., II, Gee, J. M., Robertson, G. T., Richardson, J. M., Ng, W. L., and Winkler, M. E. (2003) Brucella stationary-phase gene expression and virulence. Annu. Rev. Microbiol. 57, 57-76.
11. Lapaque, N., Moriyon, I., Moreno, E., and Gorvel, J. P. (2005) Brucella lipopolysaccharide acts as a virulence factor. Curr. Opin. Microbiol. 8, 60-66.
12. Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N., and Bourne, P. E. (2000) The Protein Data Bank. Nucleic Acids Res. 28, 235-242.
13. Karimova, G., Pidoux, J., Ullmann, A., and Ladant, D. (1998) A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc. Natl. Acad. Sci. U.S.A. 95, 5752-5756.
14. Andrade, M. A., Chacon, P., Merelo, J. J., and Moran, F. (1993) Evaluation of secondary structure of proteins from UV circular dichroism spectra using an unsupervised learning neural network. Protein Eng. 6, 383-390.
15. Pecheur, E. I., Hoekstra, D., Sainte-Marie, J., Maurin, L., Bienvenue, A., and Philippot, J. R. (1997) Membrane anchorage brings about fusogenic properties in a short synthetic peptide. Biochemistry 36, 3773-3781.
16. Duzgunes, N., and Wilschut, J. (1993) Fusion assays monitoring intermixing of aqueous contents. Methods Enzymol. 220, 3-14.
17. Finn, R. D., Mistry, J., Schuster-Bockler, B., Griffiths-Jones, S., Hollich, V., Lassmann, T., Moxon, S., Marshall, M., Khanna, A., Durbin, R., Eddy, S. R., Sonnhammer, E. L., and Bateman, A. (2006) Pfam: Clans, web tools and services. Nucleic Acids Res. 34, D247-D251.
18. Rost, B., Yachdav, G., and Liu, J. (2004) The PredictProtein server. Nucleic Acids Res. 32, W321-W326.
19. Berger, B., Wilson, D. B., Wolf, E., Tonchev, T., Milla, M., and Kim, P. S. (1995) Predicting coiled coils by use of pairwise residue correlations. Proc. Natl. Acad. Sci. U.S.A. 92, 8259-8263.
20. Mitra, N., Sinha, S., Kini, R. M., and Surolia, A. (2005) Analysis of the peanut agglutinin molten globule-like intermediate by limited proteolysis. Biochim. Biophys. Acta 1725, 283-289.
21. Kalaycioglu, S., Imren, Y., Erer, D., Zor, H., and Arman, D. (2005) Brucella endocarditis with repeated mitral valve replacement. J. Cardiovasc. Surg. 20, 189-192.
22. Romero, P., Obradovic, Z., and Dunker, A. K. (1997) Sequence Data Analysis for Long Disordered Regions Prediction in the Calcineurin Family. Genome Inf. 8, 110-124.
23. Uversky, V. N. (2002) What does it mean to be natively unfolded? Eur. J. Biochem. 269, 2-12.
24. Dutch, R. E., Jardetzky, T. S., and Lamb, R. A. (2000) Virus membrane fusion proteins: Biological machines that undergo a metamorphosis. Biosci. Rep. 20, 597-612.
25. Huang, Q., Sivaramakrishna, R. P., Ludwig, K., Korte, T., Bottcher, C., and Herrmann, A. (2003) Early steps of the conformational change of influenza virus hemagglutinin to a fusion active state: Stability and energetics of the hemagglutinin. Biochim. Biophys. Acta 1614, 3-13.
26. Trivedi, V. D., Yu, C., Veeramuthu, B., Francis, S., and Chang, D. K. (2000) Fusion induced aggregation of model vesicles studied by dynamic and static light scattering. Chem. Phys. Lipids 107, 99-106.
27. Lupas, A. (1996) Coiled coils: New structures and new functions. Trends Biochem. Sci. 21, 375-382.
28. Wolf, E., Kim, P. S., and Berger, B. (1997) MultiCoil: A program for predicting two- and three-stranded coiled coils. Protein Sci. 6, 1179-1189.
29. Kammerer, R. A., Kostrewa, D., Progias, P., Honnappa, S., Avila, D., Lustig, A., Winkler, F. K., Pieters, J., and Steinmetz, M. O. (2005) A conserved trimerization motif controls the topology of short coiled coils. Proc. Natl. Acad. Sci. U.S.A. 102, 13891-13896.
30. Woolfson, D. N., and Alber, T. (1995) Predicting oligomerization states of coiled coils. Protein Sci. 4, 1596-1607.
31. Gonzalez, L., Jr., Woolfson, D. N., and Alber, T. (1996) Buried polar residues and structural specificity in the GCN4 leucine zipper. Nat. Struct. Biol. 3, 1011-1018.
32. Eckert, D. M., Malashkevich, V. N., and Kim, P. S. (1998) Crystal structure of GCN4-pIQI, a trimeric coiled coil with buried polar residues. J. Mol. Biol. 284, 859-865.
33. White, D., Musse, A. A., Wang, J., London, E., and Merrill, A. R. (2006) Toward elucidating the membrane topology of helix two of the colicin E1 channel domain. J. Biol. Chem. 281, 32375-32384.
34. Malovrh, P., Viero, G., Serra, M. D., Podlesek, Z., Lakey, J. H., Macek, P., Menestrina, G., and Anderluh, G. (2003) A novel mechanism of pore formation: Membrane penetration by the N-terminal amphipathic region of equinatoxin. J. Biol. Chem. 278, 22678-22685.
35. Bechinger, B. (1999) The structure, dynamics and orientation of antimicrobial peptides in membranes by multidimensional solid-state NMR spectroscopy. Biochim. Biophys. Acta 1462, 157-183.
36. Pecheur, E. I., Martin, I., Ruysschaert, J. M., Bienvenue, A., and Hoekstra, D. (1998) Membrane fusion induced by 11-mer anionic and cationic peptides: A structure-function study. Biochemistry 37, 2361-2371.
37. Parente, R. A., Nir, S., and Szoka, F. C., Jr. (1988) pH-dependent fusion of phosphatidylcholine small vesicles. Induction by a synthetic amphipathic peptide. J. Biol. Chem. 263, 4724-4730.
38. Blondelle, S. E., Lohner, K., and Aguilar, M. ( 1999) Lipid-induced conformation and lipid-binding properties of cytolytic and anti-microbial peptides: Determination and biological specificity. Biochim. Biophys. Acta 1462, 89-108.
39. Hayward, R. D., McGhie, E. J., and Koronakis, V. (2000) Membrane fusion activity of purified SipB, a Salmonella surface protein essential for mammalian cell invasion. Mol. Microbiol. 37, 727-739.
40. Fasshauer, D. (2003) Structural insights into the SNARE mechanism. Biochim. Biophys. Acta 1641, 87-97.
41. Wilson, I. A., Skehel, J. J., and Wiley, D. C. (1981) Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 Å resolution. Nature 289, 366-373.
42. Fass, D., Harrison, S. C., and Kim, P. S. (1996) Retrovirus envelope domain at 1.7 angstrom resolution. Nat. Struct. Biol. 3, 465-469.
43. Chan, D. C., Fass, D., Berger, J. M., and Kim, P. S. (1997) Core structure of gp41 from the HIV envelope glycoprotein. Cell 89, 263-273.
44. Malashkevich, V. N., Chan, D. C., Chutkowski, C. T., and Kim, P. S. (1998) Crystal structure of the simian immunodeficiency virus (SIV) gp41 core: Conserved helical interactions underlie the broad inhibitory activity of gp41 peptides. Proc. Natl. Acad. Sci. U.S.A. 95, 9134-9139.
45. Malashkevich, V. N., Schneider, B. J., McNally, M. L., Milhollen, M. A., Pang, J. X., and Kim, P. S. (1999) Core structure of the envelope glycoprotein GP2 from Ebola virus at 1.9-Å resolution. Proc. Natl. Acad. Sci. U.S.A. 96, 2662-2667.
46. Gallaher, W. R. (1987) Detection of a fusion peptide sequence in the transmembrane protein of human immunodeficiency virus. Cell 50, 327-328.
47. Jahn, R., and Grubmuller, H. (2002) Membrane fusion. Curr. Opin. Cell Biol. 14, 488-495.
48. Scales, S. J., Hesser, B. A., Masuda, E. S., and Scheller, R. H. (2002) Amisyn, a novel syntaxin-binding protein that may regulate SNARE complex assembly. J. Biol. Chem. 277, 28271-28279.
49. Hatsuzawa, K., Lang, T., Fasshauer, D., Bruns, D., and Jahn, R. (2003) The R-SNARE motif of tomosyn forms SNARE core complexes with syntaxin 1 and SNAP-25 and down-regulates exocytosis. J. Biol. Chem. 278, 31159-31166.
50. Doerks, T., von Mering, C., and Bork, P. (2004) Functional clues for hypothetical proteins based on genomic context analysis in prokaryotes. Nucleic Acids Res. 32, 6321-6326.
51. Gaudermann, P., Vogl, I., Zientz, E., Silva, F. J., Moya, A., Gross, R., and Dandekar, T. (2006) Analysis of and function predictions for previously conserved hypothetical or putative proteins in Blochmannia floridanus. BMC Microbiol. 6, 1.
52. Tai, L. J., McFall, S. M., Huang, K., Demeler, B., Fox, S. G., Brubaker, K., Radhakrishnan, I., and Morimoto, R. I. (2002) Structure-function analysis of the heat shock factor-binding protein reveals a protein composed solely of a highly conserved and dynamic coiled-coil trimerization domain. J. Biol. Chem. 277, 735-745.