Spectroscopic characterization and fusogenic properties of PreS domains of duck hepatitis B virus

Biochemistry

Volumn 51, Issue 42, 2012, Pages 8444-8454

  Delgado, Carmen L ^a,c   Núñez, Elena ^a,d   Yélamos, Belén ^a   Gómez Gutiérrez, Julián ^a   Peterson, Darrell L ^b   Gavilanes, Francisco ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c ASICI Pabellón Central ^*  (Spain)

^d Janssen Cilag SA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDIC PHOSPHOLIPIDS; AMINO ACID SEQUENCE; APOLAR AMINO ACIDS; CELLULAR MEMBRANES; CONFORMATIONAL FLEXIBILITY; FLUORESCENCE POLARIZATION; FUSION MECHANISM; FUSION PROCESS; HEPATITIS B VIRUS; INTEGRAL MEMBRANE PROTEINS; IONIC INTERACTION; LIPID MIXING; N-TERMINALS; PHOSPHOLIPID VESICLES; POLAR HEADGROUPS; PRE-S REGION; SPECTROSCOPIC CHARACTERIZATION; THREE-DIMENSIONAL STRUCTURE; TRANSITION ENTHALPY;

AMINO ACIDS; CELL MEMBRANES; CIRCULAR DICHROISM SPECTROSCOPY; FLUORESCENCE; LIPOSOMES; PHOSPHOLIPIDS; VIRUSES;

RECOMBINANT PROTEINS;

HISTIDINE DERIVATIVE; MEMBRANE PROTEIN; PHOSPHOLIPID; PRES PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; CONTROLLED STUDY; ENTHALPY; FLUORESCENCE SPECTROSCOPY; HEPATITIS B VIRUS; NONHUMAN; PHOSPHOLIPID VESICLE; POLARIZATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; TRANSITION TEMPERATURE;

CIRCULAR DICHROISM; CLONING, MOLECULAR; HEPATITIS B VIRUS, DUCK; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LIPOSOMES; PHOSPHOLIPIDS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; VIRAL ENVELOPE PROTEINS; VIRAL FUSION PROTEINS; VIRUS INTERNALIZATION;

EID: 84867786488     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi3008406     Document Type: Article

References (50)

1. Breiner, K. M., Urban, S., and Schaller, H. (1998) Carboxypeptidase D (gp180), a Golgi-resident protein, functions in the attachment and entry of avian hepatitis B viruses J. Virol. 72, 8098-8104
2. Tong, S., Li, J., and Wands, J. R. (1999) Carboxypeptide D is an avian hepatitis B virus receptor J. Virol. 73, 8696-8702
3. Li, J., Tong, S., Lee, H. B., Perdigoto, A. L., Spangenberg, H. C., and Wands, J. R. (2004) Glycine decarboxylase mediates a postbinding step in duck hepatitis B virus infection J. Virol. 78, 1873-1881
4. Funk, A., Mhamdi, M., Hohenberg, H., Will, H., and Sirma, H. (2006) pH-independent entry and sequential endosomal sorting are major determinants of hepadnaviral infection in primary hepatocytes Hepatology 44, 685-693
5. Chojnacki, J., Anderson, D. A., and Grgacic, E. V. L (2005) A hydrophobic domain in the large envelope protein is essential for fusion of duck hepatitis B virus at the late endosome J. Virol. 79, 14945-14955
6. Glebe, D. and Urban, S. (2007) Viral and cellular determinants involved in hepadnaviral entry World J. Gastroenterol. 13, 22-38
7. Zhang, X., Lin, S. M., Chen, T. Y., Liu, M., Ye, F., Chen, Y. R., Shi, L., He, Y. L., Wu, L. X., Zheng, S. Q., Zhao, Y. R., and Zhang, S. L. (2011) Asialoglycoprotein receptor interacts with the preS1 domain of hepatitis B virus in vivo and in vitro Arch. Virol. 156, 637-645
8. Sunyach, C., Rollier, C., Robaczewska, M., Borel, C., Barraid, L., Kay, A., Trépo, C., Will, H., and Cova, L. (1999) Residues critical for Duck Hepatitis B Virus neutralization are involved in host cell interaction J. Virol. 73, 2569-2575
9. Grgacic, E. V. L and Anderson, D. A. (2005) S-t, a truncated envelope protein derived from the S protein of duck hepatitis B virus, acts as a chaperone for the folding of the large envelope protein J. Virol. 79, 5346-5352
10. Urban, S., Breiner, K. M., Fehler, F., Klingmüller, U., and Schaller, H. (1998) Avian hepatitis B virus infection is initiated by the interaction of a distinct preS subdomain with the cellular receptor gp180 J. Virol. 72, 8089-8097
11. Guo, J. T. and Pugh, J. C. (1997) Topology of the large envelope protein of duck hepatitis B virus suggests a mechanism for membrane translocation during particle morphogenesis J. Virol. 71, 1107-1114
12. Rodríguez-Crespo, I., Núñez, E., Gómez- Gutiérrez, J., Yélamos, B., Albar, J. P., Peterson, D. L., and Gavilanes, F. (1995) Phospholipid interactions of a putative fusion peptide of hepatitis B virus surface antigen S protein J. Gen. Virol. 76, 301-308
13. Rodríguez-Crespo, I., Gómez-Gutiérrez, J., Encinar, J. A., González-Ros, J. M., Albar, J. P., Peterson, D. L., and Gavilanes, F. (1996) Structural properties of the putative fusion peptide of hepatitis B virus upon interaction with phospholipids. Circular dichroism and Fourier-transform infrared spectroscopy studies Eur. J. Biochem. 242, 243-248
14. Rodríguez-Crespo, I., Núñez, E., Yélamos, B., Gómez-Gutiérrez, J., Albar, J. P., Peterson, D. L., and Gavilanes, F. (1999) Fusogenic activity of hepadnavirus peptides corresponding to sequences downstream of the putative cleavage site Virology 261, 133-142
15. Lu, X., Hazboun, T., and Block, T. (2001) Limited proteolysis induces woodchuck hepatitis virus infectivity for human HepG2 cells Virus Res. 73, 27-40
16. Maenz, C., Chang, S. F., Iwanski, A., and Bruns, M. (2007) Entry of duck hepatitis B virus into primary duck liver and kidney cells after discovery of a fusogenic region within the large surface protein J. Virol. 81, 5014-5023
17. Núñez, E., Yélamos, B., Delgado, C., Gómez-Gutiérrez, J., Peterson, D. L., and Gavilanes, F. (2008) Interaction of preS domains of hepatitis B virus with phospholipid vesicles Biochim. Biophys. Acta 17884, 417-424
18. Stoeckl, L., Funk, A., Kopitzki, A., Brandenburg, B., Oess, S., Will, H., Sirma, H., and Hildt, E. (2006) Identification of a structural motif crucial for infectivity of hepatitis B viruses Proc. Natl. Acad. Sci. U. S. A. 103, 6730-6734
19. Blanchet, M. and Sureau, C. (2007) Infectivity determinants of the hepatitis B virus pre-S domain are confined to the N-terminal 75 amino acid residues J. Virol. 81, 5841-5849
20. Gudima, S., Meier, A., Dunbrack, R., Taylor, J., and Bruss, V. (2007) Two potentially important elements of the hepatitis B virus large envelope protein are dispensable for the infectivity of hepatitis delta virus J. Virol. 81, 4343-4347
21. Ni, Y., Sonnabend, J., Seitz, S., and Urban, S. (2010) The pre-s2 domain of the hepatitis B virus is dispensable for infectivity but serves a spacer function for L-protein-connected virus assembly J. Virol. 84, 3879-3888
22. Núñez, E., Wei, X., Delgado, C., Rodríguez-Crespo, I., Yélamos, B., Gómez-Gutiérrez, J., Peterson, D. L., and Gavilanes, F. (2001) Cloning, expression, and purification of histidine-tagged preS domains of hepatitis B virus Protein Expr. Purif. 21, 183-191
23. Perczel, A., Hollósi, M., Tusnády, G., and Fasman, G. D. (1991) Decovolution of the circular dichroism spectra of proteins: The circular dichroism spectra of antiparallel -sheet in proteins Protein Eng. 4, 669-679
24. Rapaport, D. and Shai, Y. (1991) Interaction of fluorescently labeled pardaxin and its analogues with lipid bilayers J. Biol. Chem. 266, 23769-23775
25. Struck, D. K., Hoekstra, D., and Pagano, R. E. (1981) Use of resonance energy transfer to monitor membrane fusion Biochemistry 20, 4093-4099
26. 2+-induced fusion and destabilization of liposomes Biochemistry 24, 3099-3106
27. Rajarathnam, K., Hochman, J., Schindler, M., and Ferguson-Miller, S. (1989) Synthesis, location, and lateral mobility of fluorescently labeled ubiquinone 10 in mitochondrial and artificial membranes Biochemistry 28, 3168-3176
28. Blumenthal, R., Henkart, M., and Steer, C. J. (1983) Clathrin-induced pH-dependent fusion of phosphatidylcholine vesicles J. Biol. Chem. 258, 3409-3415
29. Rapaport, D. and Shai, Y. (1994) Interaction of fluorescently labeled analogues of the amino-terminal fusion peptide of Sendai virus with phospholipid membranes J. Biol. Chem. 269, 15124-15131
30. Schwarz, G., Gerke, H., Rizzo, V., and Stankowski, S. (1987) Incorporation kinetics in a membrane, studied with the pore-forming peptide alamethicin Biophys. J. 52, 685-692
31. Papahadjopoulos, D., Moscarello, M., Eylar, E. H., and Isac, T. (1975) Effects of proteins on thermotropic phase transitions of phospholipid membranes Biochim. Biophys. Acta 401, 317-335
32. Lentz, B. R., Barenholz, Y., and Thompson, T. E. (1976) Fluorescence depolarization studies of phase transitions and fluidity in phospholipid bilayers. 2 Two-component phosphatidylcholine liposomes Biochemistry 15, 4529-4537
33. Prendergast, F. G., Haugland, R. P., and Callahan, P. J. (1981) 1-[4-(Trimethylamino)phenyl]-6-phenylhexa-1,3,5-triene: synthesis, fluorescence properties, and use as a fluorescence probe of lipid bilayers Biochemistry 20, 7333-7338
34. Mao, D. and Wallace, B. A. (1984) Differential light scattering and absorption flattening optical effects are minimal in the circular dichroism spectra of small unilamellar vesicles Biochemistry 23, 2667-2673
35. Wimley, W. C. and White, S. H. (2000) Designing Transmembrane α-Helices That Insert Spontaneously Biochemistry 39, 4432-4442
36. Horniak, L., Pilon, M., van 't Hof, R., and de Kruijff, B. (1993) The secondary structure of the ferredoxin transit sequence is modulated by its interaction with negatively charged lipids FEBS Lett. 334, 241-246
37. Bullough, P. A., Hughson, F. M., Skehel, J. J., and Wiley, D. C. (1994) Structure of influenza haemagglutinin at the pH of membrane fusion Nature 371, 37-43
38. Nieva, J. L., Nir, S., and Wilschut, J. (1998) Destabilization and fusion of zwitteronic large unilamellar lipid vesicles induced by a β-type structure of the HIV-1 fusion peptide J. Liposome Res. 8, 165-182
39. Davies, S. M., Epand, R. F., Bradshaw, J. P., and Epand, R. M. (1998) Modulation of lipid polymorphism by the feline leukemia virus fusion peptide: implications for the fusion mechanism Biochemistry 37, 5720-5729
40. Callebaut, I., Tasso, A., Brasseur, R., Burny, A., Portetelle, D., and Mornon, J. P. (1994) Common prevalence of alanine and glycine in mobile reactive centre loops of serpins and viral fusion peptides: do prions possess a fusion peptide? J. Comput. Aided Mol. Des. 8, 175-191
41. Nir, S. and Nieva, J. L. (2000) Interactions of peptides with liposomes: pore formation and fusion Prog. Lipid Res. 39, 181-206
42. Duzgunes, N. and Shavnin, S. A. (1992) Membrane destabilization by N-terminal peptides of viral envelope proteins J. Membr. Biol. 128, 71-80
43. Samuel, O. and Shai, Y. (2001) Participation of two fusion peptides in measles virus-induced membrane fusion: emerging similarity with other paramyxoviruses Biochemistry 40, 1340-1349
44. Stegmann, T., Hoekstra, D., Scherphof, G., and Wilschut, J. (1986) Fusion activity of influenza virus. A comparison between biological and artificial target membrane vesicles J. Biol. Chem. 261, 10966-10969
45. Lavillette, D., Pecheur, E. I., Donot, P., Fresquet, J., Molle, J., Corbau, R., Dreux, M., Penin, F., and Cosset, F. L. (2007) Characterization of fusion determinants points to the involvement of three discrete regions of both E1 and E2 glycoproteins in the membrane fusion process of hepatitis C virus J. Virol. 81, 8752-8765
46. Pacheco, B., Gómez-Gutiérrez, J., Yélamos, B., Delgado, C., Roncal, F., Albar, J. P., Peterson, D., and Gavilanes, F. (2006) Membrane-perturbing properties of three peptides corresponding to the ectodomain of hepatitis C virus E2 envelope protein Biochim. Biophys. Acta 1758, 755-763
47. Pérez-Berna, A. J., Guillén, J., Moreno, M. R., Gómez-Sánchez, A. I., Pabst, G., Laggner, P., and Villalaín, J. (2008) Interaction of the most membranotropic region of the HCV E2 envelope glycoprotein with membranes. Biophysical characterization Biophys. J. 94, 4737-4750
48. Gray, C., Tatulian, S. A., Wharton, S. A., and Tamm, L. K. (1996) Effect of the N-terminal glycine on the secondary structure, orientation, and interaction of the influenza hemagglutinin fusion peptide with lipid bilayers Biophys. J. 70, 2275-2286
49. Peisajovich, S. G., Epand, R. F., Pritsker, M., Shai, Y., and Epand, R. M. (2000) The polar region consecutive to the HIV fusion peptide participates in membrane fusion Biochemistry 39, 1826-1833
50. Eisenberg, D., Schwarz, E., Komaromy, M., and Wall, R. (1984) Analysis of membrane and surface protein sequences with the hydrophobic moment plot J. Mol. Biol. 179, 125-142