Intracellular trafficking of bio-nanocapsule-liposome complex: Identification of fusogenic activity in the pre-S1 region of hepatitis B virus surface antigen L protein

Journal of Controlled Release

Volumn 212, Issue , 2015, Pages 10-18

  Somiya, Masaharu ^a,b   Sasaki, Yasuo ^c   Matsuzaki, Takashi ^c   Liu, Qiushi ^a,c   Iijima, Masumi ^a   Yoshimoto, Nobuo ^a   Niimi, Tomoaki ^a   Maturana, Andrés Daniel ^a   Kuroda, Shun'Ichi ^a,c  

^a NAGOYA UNIVERSITY   (Japan)

^b JAPAN SOCIETY FOR THE PROMOTION OF SCIENCE   (Japan)

^c OSAKA UNIVERSITY   (Japan)

Author keywords

Bio nanocapsules; Drug delivery; Endosomal escape; Fusogenic activity; Hepatitis B virus surface antigen; Liposomes

Indexed keywords

ANTIGENS; CELL MEMBRANES; CELLS; DRUG DELIVERY; GENE TRANSFER; GENES; LIPOSOMES; MOLECULAR BIOLOGY; NANOCAPSULES; PROTEINS; VIRUSES;

BIO NANOCAPSULES; ENDOSOMAL ESCAPES; ENDOSOMAL MEMBRANE; GENE DELIVERY SYSTEMS; HEPATITIS B VIRUS SURFACE ANTIGENS; HOLLOW NANOPARTICLES; INTRACELLULAR TRAFFICKING; TRANS-MEMBRANE PROTEINS;

CYTOLOGY;

DIHYDROLIPOAMIDE DEHYDROGENASE; DOXORUBICIN; LIPOSOME; NANOCAPSULE; VIRUS ANTIGEN; L PROTEIN, HEPATITIS B VIRUS; VIRUS ENVELOPE PROTEIN;

ARTICLE; CONTROLLED STUDY; CYTOPLASM; DRUG ACTIVITY; DRUG IDENTIFICATION; DRUG RELEASE; ENDOCYTOSIS; FUSOGENIC ACTIVITY; GENE TARGETING; HEPATITIS B; HEPATITIS B VIRUS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL; MEMBRANE FUSION; NONHUMAN; PH; PRIORITY JOURNAL; ANIMAL; CHEMISTRY; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; MOUSE; SACCHAROMYCES CEREVISIAE; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; COS CELLS; ENDOCYTOSIS; HUMANS; LIPOSOMES; MICE; NANOCAPSULES; SACCHAROMYCES CEREVISIAE; VIRAL ENVELOPE PROTEINS;

EID: 84935879671     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2015.06.012     Document Type: Article

References (40)

1. A.R. Neurath, S.B. Kent, N. Strick, and K. Parker Identification and chemical synthesis of a host cell receptor binding site on hepatitis B virus Cell 46 1986 429 436 10.1016/0092-8674(86)90663-X (pii)
2. S. Kuroda, S. Otaka, T. Miyazaki, M. Nakao, and Y. Fujisawa Hepatitis B virus envelope L protein particles: synthesis and assembly in Saccharomyces cerevisiae, purification and characterization J. Biol. Chem. 267 1992 1953 1961 (http://www.ncbi.nlm.nih.gov/pubmed/18434744)
3. T. Yamada, H. Iwabuki, T. Kanno, H. Tanaka, T. Kawai, and H. Fukuda Physicochemical and immunological characterization of hepatitis B virus envelope particles exclusively consisting of the entire L (pre-S1 + pre-S2 + S) protein Vaccine 19 2001 3154 3163 10.1016/S0264-410X(01)00017-2
4. M. Yamada, A. Oeda, J. Jung, M. Iijima, N. Yoshimoto, and T. Niimi Hepatitis B virus envelope L protein-derived bio-nanocapsules: mechanisms of cellular attachment and entry into human hepatic cells J. Control. Release 160 2012 322 329 10.1016/j.jconrel.2011.11.004
5. T. Yamada, Y. Iwasaki, H. Tada, H. Iwabuki, M.K.L. Chuah, and T. VandenDriessche Nanoparticles for the delivery of genes and drugs to human hepatocytes Nat. Biotechnol. 21 2003 885 890 10.1038/nbt843
6. Y. Iwasaki, M. Ueda, T. Yamada, A. Kondo, M. Seno, and K. Tanizawa Gene therapy of liver tumors with human liver-specific nanoparticles Cancer Gene Ther. 14 2007 74 81 10.1038/sj.cgt.7700990
7. Y. Kaneda Virosomes: evolution of the liposome as a targeted drug delivery system Adv. Drug Deliv. Rev. 43 2000 197 205 10.1016/S0169-409X(00)00069-7
8. J. Jung, T. Matsuzaki, K. Tatematsu, T. Okajima, K. Tanizawa, and S. Kuroda Bio-nanocapsule conjugated with liposomes for in vivo pinpoint delivery of various materials J. Control. Release 126 2008 255 264 10.1016/j.jconrel.2007.12.002
9. J. Jung, M. Iijima, N. Yoshimoto, M. Sasaki, T. Niimi, and K. Tatematsu Efficient and rapid purification of drug- and gene-carrying bio-nanocapsules, hepatitis B virus surface antigen L particles, from Saccharomyces cerevisiae Protein Expr. Purif. 78 2011 149 155 10.1016/j.pep.2011.04.008
10. G. Sauerbrey The use of quartz oscillators for weighing thin layers and for microweighing Z. Phys. 155 1959 206 222 10.1007/BF01337937
11. H.T.S. Britton, and R.A. Robinson CXCVIII. Universal buffer solutions and the dissociation constant of veronal J. Chem. Soc. 1923 1456 1462 10.1039/JR9310001456
12. T. Kasuya, J. Jung, R. Kinoshita, Y. Goh, T. Matsuzaki, and M. Iijima Bio-nanocapsule-liposome conjugates for in vivo pinpoint drug and gene delivery Methods Enzymol. 464 2009 147 166 10.1016/S0076-6879(09)64008-8
13. X. Li, D.J. Hirsh, D. Cabral-Lilly, A. Zirkel, S.M. Gruner, and A.S. Janoff Doxorubicin physical state in solution and inside liposomes loaded via a pH gradient Biochim. Biophys. Acta Biomembr. 1415 1998 23 40 10.1016/S0005-2736(98)00175-8
14. E. Yuba, A. Harada, Y. Sakanishi, S. Watarai, and K. Kono A liposome-based antigen delivery system using pH-sensitive fusogenic polymers for cancer immunotherapy Biomaterials 34 2013 3042 3052 10.1016/j.biomaterials.2012.12.031
15. H. Ellens, J. Bentz, and F.C. Szoka H +- and Ca2 +-induced fusion and destabilization of liposomes Biochemistry 24 1985 3099 3106 10.1021/bi00334a005
16. J. Bhattacharya, U. Choudhuri, O. Siwach, P. Sen, and A.K. Dasgupta Interaction of hemoglobin and copper nanoparticles: implications in hemoglobinopathy Nanomedicine 2 2006 191 199 10.1016/j.nano.2006.07.001
17. V.S. Malinin, P. Frederik, and B.R. Lentz Osmotic and curvature stress affect PEG-induced fusion of lipid vesicles but not mixing of their lipids Biophys. J. 82 2002 2090 2100 10.1016/S0006-3495(02)75556-2
18. S.M. Dennison, M.E. Bowen, A.T. Brunger, and B.R. Lentz Neuronal SNAREs do not trigger fusion between synthetic membranes but do promote PEG-mediated membrane fusion Biophys. J. 90 2006 1661 1675 10.1529/biophysj.105.069617
19. E.V.L. Grgacic, and H. Schaller A metastable form of the large envelope protein of duck hepatitis B virus: low-pH release results in a transition to a hydrophobic, potentially fusogenic conformation J. Virol. 74 2000 5116 5122 10.1128/JVI.74.11.5116-5122.2000
20. J. Petersen, M. Dandri, W. Mier, M. Lütgehetmann, T. Volz, and F. von Weizsäcker Prevention of hepatitis B virus infection in vivo by entry inhibitors derived from the large envelope protein Nat. Biotechnol. 26 2008 335 341 10.1038/nbt1389
21. J. White Membrane fusion Science 258 1992 917 924 10.1126/science.1439803 (80-.)
22. F.M. Hughson Structural characterization of viral fusion proteins Curr. Biol. 5 1995 265 274 10.1016/S0960-9822(95)00057-1
23. M. Kielian, and F. a Rey Virus membrane-fusion proteins: more than one way to make a hairpin Nat. Rev. Microbiol. 4 2006 67 76 10.1038/nrmicro1326
24. S.C. Harrison Viral membrane fusion Nat. Struct. Mol. Biol. 15 2008 690 698 10.1038/nsmb.1456
25. X. Lu, and T. Block Study of the early steps of the hepatitis B virus life cycle Int. J. Med. Sci. 1 2004 21 33
26. A. Cooper The earliest steps in hepatitis B virus infection Biochim. Biophys. Acta Biomembr. 1614 2003 89 96 10.1016/S0005-2736(03)00166-4
27. I. Rodriguez-Crespo, J. Gomez-Gutierrez, M. Nieto, D.L. Peterson, and F. Gavilanes Prediction of a putative fusion peptide in the S protein of hepatitis B virus J. Gen. Virol. 75 1994 637 639 10.1099/0022-1317-75-3-637
28. S. Oess, and E. Hildt Novel cell permeable motif derived from the PreS2-domain of hepatitis-B virus surface antigens Gene Ther. 7 2000 750 758 10.1038/sj.gt.3301154
29. I. Rodriguez-Crespo, E. Nunez, J. Gomez-Gutierrez, B. Yelamos, J.P. Albar, and D.L. Peterson Phospholipid interactions of the putative fusion peptide of hepatitis B virus surface antigen S protein J. Gen. Virol. 76 1995 301 308 10.1099/0022-1317-76-2-301
30. M. Engelke, K. Mills, S. Seitz, P. Simon, P. Gripon, and M. Schnölzer Characterization of a hepatitis B and hepatitis delta virus receptor binding site Hepatology 43 2006 750 760 10.1002/hep.21112
31. E. Wisse, F. Jacobs, B. Topal, P. Frederik, and B. De Geest The size of endothelial fenestrae in human liver sinusoids: implications for hepatocyte-directed gene transfer Gene Ther. 15 2008 1193 1199 10.1038/gt.2008.60
32. C.E. Futter, A. Pearse, L.J. Hewlett, and C.R. Hopkins Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes J. Cell Biol. 132 1996 1011 1023 10.1083/jcb.132.6.1011
33. L.H. Wang, K.G. Rothberg, and R.G.W. Anderson Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation J. Cell Biol. 123 1993 1107 1117 10.1083/jcb.123.5.1107
34. M.A. West, and S. Bretscher Distinct endocytotic pathways in epidermal growth factor-stimulated human carcinoma A431 cells [published erratum appears in J Cell Biol 1990 Mar;110(3):859] 109 1989 2731 2739 10.1083/jcb.109.6.2731
35. R. Mayoral, A.M. Valverde, C. Llorente Izquierdo, A. González-Rodríguez, L. Boscá, and P. Martín-Sanz Impairment of transforming growth factor beta signaling in caveolin-1-deficient hepatocytes: role in liver regeneration J. Biol. Chem. 285 2010 3633 3642 10.1074/jbc.M109.072900
36. J.A. Swanson, and C. Watts Macropinocytosis Trends Cell Biol. 5 1995 424 428 10.1016/S0962-8924(00)89101-1
37. S. Schädler, and E. Hildt HBV life cycle: entry and morphogenesis Viruses 1 2009 185 209 10.3390/v1020185
38. A. Schulze, P. Gripon, and S. Urban Hepatitis B virus infection initiates with a large surface protein-dependent binding to heparan sulfate proteoglycans Hepatology 46 2007 1759 1768 10.1002/hep.21896
39. H. Yan, G. Zhong, G. Xu, W. He, Z. Jing, and Z. Gao Sodium taurocholate cotransporting polypeptide is a functional receptor for human hepatitis B and D virus eLife 1 2012 e00049 10.7554/eLife.00049
40. J. Schneider-Schaulies Cellular receptors for viruses: links to tropism and pathogenesis J. Gen. Virol. 81 2000 1413 1429 (http://www.ncbi.nlm.nih.gov/pubmed/10811925)