Potent Inhibition of Late Stages of Hepadnavirus Replication by a Modified Cell Penetrating Peptide

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Abdul, Fabien ^a,b,c   Ndeboko, Bénédicte ^a,b,c   Buronfosse, Thierry ^a,b,c,d   Zoulim, Fabien ^a,b,c   Kann, Michael ^e,f,g   Nielsen, Peter E ^h   Cova, Lucyna ^a,b,c  

^a UNIVERSITÉ LYON 1   (France)

^b INSERM   (France)

^c CENTRE DE RECHERCHE EN CANCÉROLOGIE DE LYON   (France)

^d VETAGRO SUP   (France)

^e UNIVERSITÉ DE BORDEAUX   (France)

^f CNRS   (France)

^g BORDEAUX UNIVERSITY HOSPITAL   (France)

^h UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PENETRATING PEPTIDE; ENVELOPE PROTEIN; VIRUS DNA; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DUCK HEPATITIS B VIRUS; HEPADNAVIRUS; NONHUMAN; SUCROSE GRADIENT; SUPERNATANT; VIRION; VIRUS ENTRY; VIRUS INHIBITION; VIRUS MORPHOGENESIS; VIRUS NUCLEOCAPSID; VIRUS PARTICLE; VIRUS RELEASE; VIRUS REPLICATION;

ANIMALS; CAPSID; CELL LINE; CELL-PENETRATING PEPTIDES; GENE EXPRESSION REGULATION, VIRAL; HEPATITIS B VIRUS, DUCK; HUMANS; INTRACELLULAR SPACE; LIPID METABOLISM; PROTEIN TRANSPORT; TIME FACTORS; VIRAL STRUCTURAL PROTEINS; VIRUS REPLICATION;

DUCK HEPATITIS B VIRUS; HEPADNAVIRIDAE; HEPATITIS B VIRUS;

EID: 84869224998     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0048721     Document Type: Article

References (63)

1. Holm T, Johansson H, Lundberg P, Pooga M, Lindgren M, et al. (2006) Studying the uptake of cell-penetrating peptides. Nat Protoc 1: 1001-1005.
2. Schmidt N, Mishra A, Lai GH, Wong GC (2009) Arginine-rich cell-penetrating peptides. FEBS Lett.
3. Guterstam P, Madani F, Hirose H, Takeuchi T, Futaki S, et al. (2009) Elucidating cell-penetrating peptide mechanisms of action for membrane interaction, cellular uptake, and translocation utilizing the hydrophobic counter-anion pyrenebutyrate. Biochim Biophys Acta 1788: 2509-2517.
4. Tunnemann G, Ter-Avetisyan G, Martin RM, Stockl M, Herrmann A, et al. (2008) Live-cell analysis of cell penetration ability and toxicity of oligo-arginines. J Pept Sci 14: 469-476.
5. Mae M, Langel U, (2006) Cell-penetrating peptides as vectors for peptide, protein and oligonucleotide delivery. Curr Opin Pharmacol 6: 509-514.
6. Bendifallah N, Rasmussen FW, Zachar V, Ebbesen P, Nielsen PE, et al. (2006) Evaluation of cell-penetrating peptides (CPPs) as vehicles for intracellular delivery of antisense peptide nucleic acid (PNA). Bioconjug Chem 17: 750-758.
7. Zorko M, Langel U, (2005) Cell-penetrating peptides: mechanism and kinetics of cargo delivery. Adv Drug Deliv Rev 57: 529-545.
8. Brown KL, Hancock RE, (2006) Cationic host defense (antimicrobial) peptides. Curr Opin Immunol 18: 24-30.
9. Hancock RE, Sahl HG, (2006) Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat Biotechnol 24: 1551-1557.
10. Jenssen H, Hamill P, Hancock RE, (2006) Peptide antimicrobial agents. Clin Microbiol Rev 19: 491-511.
11. Hancock RE, (2001) Cationic peptides: effectors in innate immunity and novel antimicrobials. Lancet Infect Dis 1: 156-164.
12. Lizzi AR, Carnicelli V, Clarkson MM, Di Giulio A, Oratore A, (2009) Lactoferrin derived peptides: mechanisms of action and their perspectives as antimicrobial and antitumoral agents. Mini Rev Med Chem 9: 687-695.
13. Marcellin P, (2009) Hepatitis B and hepatitis C in 2009. Liver Int 29 (Suppl 1): 1-8.
14. Lavanchy D, (2004) Hepatitis B virus epidemiology, disease burden, treatment, and current and emerging prevention and control measures. J Viral Hepat 11: 97-107.
15. Tillmann HL, (2007) Antiviral therapy and resistance with hepatitis B virus infection. World J Gastroenterol 13: 125-140.
16. Glebe D, Urban S, (2007) Viral and cellular determinants involved in hepadnaviral entry. World J Gastroenterol 13: 22-38.
17. Rabe B, Glebe D, Kann M, (2006) Lipid-mediated introduction of hepatitis B virus capsids into nonsusceptible cells allows highly efficient replication and facilitates the study of early infection events. J Virol 80: 5465-5473.
18. Rabe B, Vlachou A, Pante N, Helenius A, Kann M, (2003) Nuclear import of hepatitis B virus capsids and release of the viral genome. Proc Natl Acad Sci U S A 100: 9849-9854.
19. Beck J, Nassal M, (2007) Hepatitis B virus replication. World J Gastroenterol 13: 48-64.
20. Kann M, Schmitz A, Rabe B, (2007) Intracellular transport of hepatitis B virus. World J Gastroenterol 13: 39-47.
21. Seeger C, Mason WS, (2000) Hepatitis B virus biology. Microbiol Mol Biol Rev 64: 51-68.
22. Bruss V, (2007) Hepatitis B virus morphogenesis. World J Gastroenterol 13: 65-73.
23. Watanabe T, Sorensen EM, Naito A, Schott M, Kim S, et al. (2007) Involvement of host cellular multivesicular body functions in hepatitis B virus budding. Proc Natl Acad Sci U S A 104: 10205-10210.
24. Mabit H, Schaller H, (2000) Intracellular hepadnavirus nucleocapsids are selected for secretion by envelope protein-independent membrane binding. J Virol 74: 11472-11478.
25. Nassal M, (1992) The arginine-rich domain of the hepatitis B virus core protein is required for pregenome encapsidation and productive viral positive-strand DNA synthesis but not for virus assembly. J Virol 66: 4107-4116.
26. Bardens A, Doring T, Stieler J, Prange R, (2011) Alix regulates egress of hepatitis B virus naked capsid particles in an ESCRT-independent manner. Cell Microbiol 13: 602-619.
27. Rollier C, Sunyach C, Barraud L, Madani N, Jamard C, et al. (1999) Protective and therapeutic effect of DNA-based immunization against hepadnavirus large envelope protein. Gastroenterology 116: 658-665.
28. Cova L, Zoulim F, (2004) Duck hepatitis B virus model in the study of hepatitis B virus. Methods Mol Med 96: 261-268.
29. Zoulim F, Saade F, Buronfosse T, Abdul F, Cova L (2008) Hepatitis B virus, Chapter 6: Animal models for the study of HBV infection. London; Atlanta: International Medical Press.
30. Khawaja G, Buronfosse T, Jamard C, Guerret S, Zoulim F, et al. (2012) Enhanced magnitude and breadth of neutralizing humoral response to a DNA vaccine targeting the DHBV envelope protein delivered by in vivo electroporation. Virology 425: 61-69.
31. Gares SL, Fischer KP, Congly SE, Lacoste S, Addison WR, et al. (2006) Immunotargeting with CD154 (CD40 ligand) enhances DNA vaccine responses in ducks. Clin Vaccine Immunol 13: 958-965.
32. Le Guerhier F, Pichoud C, Guerret S, Chevallier M, Jamard C, et al. (2000) Characterization of the antiviral effect of 2',3'-dideoxy-2', 3'-didehydro-beta-L-5-fluorocytidine in the duck hepatitis B virus infection model. Antimicrob Agents Chemother 44: 111-122.
33. Zoulim F, Dannaoui E, Borel C, Hantz O, Lin TS, et al. (1996) 2',3'-dideoxy-beta-L-5-fluorocytidine inhibits duck hepatitis B virus reverse transcription and suppresses viral DNA synthesis in hepatocytes, both in vitro and in vivo. Antimicrob Agents Chemother 40: 448-453.
34. Nielsen PE, (2005) Addressing the challenges of cellular delivery and bioavailability of peptide nucleic acids (PNA). Q Rev Biophys 38: 345-350.
35. Robaczewska M, Narayan R, Seigneres B, Schorr O, Thermet A, et al. (2005) Sequence-specific inhibition of duck hepatitis B virus reverse transcription by peptide nucleic acids (PNA). J Hepatol 42: 180-187.
36. Shiraishi T, Nielsen PE, (2011) Improved cellular uptake of antisense peptide nucleic acids by conjugation to a cell-penetrating peptide and a lipid domain. Methods Mol Biol 751: 209-221.
37. Condreay LD, Aldrich CE, Coates L, Mason WS, Wu TT, (1990) Efficient duck hepatitis B virus production by an avian liver tumor cell line. J Virol 64: 3249-3258.
38. Gong SS, Jensen AD, Wang H, Rogler CE, (1995) Duck hepatitis B virus integrations in LMH chicken hepatoma cells: identification and characterization of new episomally derived integrations. J Virol 69: 8102-8108.
39. Koppelhus U, Shiraishi T, Zachar V, Pankratova S, Nielsen PE, (2008) Improved cellular activity of antisense peptide nucleic acids by conjugation to a cationic peptide-lipid (CatLip) domain. Bioconjug Chem 19: 1526-1534.
40. Kock J, Rosler C, Zhang JJ, Blum HE, Nassal M, et al. (2010) Generation of covalently closed circular DNA of hepatitis B viruses via intracellular recycling is regulated in a virus specific manner. PLoS Pathog 6: e1001082.
41. Bruss V, (2004) Envelopment of the hepatitis B virus nucleocapsid. Virus Res 106: 199-209.
42. Lambert C, Doring T, Prange R, (2007) Hepatitis B virus maturation is sensitive to functional inhibition of ESCRT-III, Vps4, and gamma 2-adaptin. J Virol 81: 9050-9060.
43. Mhamdi M, Funk A, Hohenberg H, Will H, Sirma H, (2007) Assembly and budding of a hepatitis B virus is mediated by a novel type of intracellular vesicles. Hepatology 46: 95-106.
44. Rabe B, Delaleau M, Bischof A, Foss M, Sominskaya I, et al. (2009) Nuclear entry of hepatitis B virus capsids involves disintegration to protein dimers followed by nuclear reassociation to capsids. PLoS Pathog 5: e1000563.
45. Noiva R, Lennarz WJ, (1992) Protein disulfide isomerase. A multifunctional protein resident in the lumen of the endoplasmic reticulum. J Biol Chem 267: 3553-3556.
46. Jenssen H, Andersen JH, Mantzilas D, Gutteberg TJ, (2004) A wide range of medium-sized, highly cationic, alpha-helical peptides show antiviral activity against herpes simplex virus. Antiviral Res 64: 119-126.
47. Jenssen H, Andersen JH, Uhlin-Hansen L, Gutteberg TJ, Rekdal O, (2004) Anti-HSV activity of lactoferricin analogues is only partly related to their affinity for heparan sulfate. Antiviral Res 61: 101-109.
48. Snijder B, Pelkmans L, (2011) Origins of regulated cell-to-cell variability. Nat Rev Mol Cell Biol 12: 119-125.
49. Snijder B, Sacher R, Ramo P, Damm EM, Liberali P, et al. (2009) Population context determines cell-to-cell variability in endocytosis and virus infection. Nature 461: 520-523.
50. Andersen JH, Jenssen H, Sandvik K, Gutteberg TJ, (2004) Anti-HSV activity of lactoferrin and lactoferricin is dependent on the presence of heparan sulphate at the cell surface. J Med Virol 74: 262-271.
51. Galdiero S, Falanga A, Vitiello M, D'Isanto M, Cantisani M, et al. (2008) Peptides containing membrane-interacting motifs inhibit herpes simplex virus type 1 infectivity. Peptides 29: 1461-1471.
52. Patient R, Hourioux C, Roingeard P, (2009) Morphogenesis of hepatitis B virus and its subviral envelope particles. Cell Microbiol 11: 1561-1570.
53. Lambert C, Prange R, (2001) Dual topology of the hepatitis B virus large envelope protein: determinants influencing post-translational pre-S translocation. J Biol Chem 276: 22265-22272.
54. Huovila AP, Eder AM, Fuller SD, (1992) Hepatitis B surface antigen assembles in a post-ER, pre-Golgi compartment. J Cell Biol 118: 1305-1320.
55. Mandart E, Kay A, Galibert F, (1984) Nucleotide sequence of a cloned duck hepatitis B virus genome: comparison with woodchuck and human hepatitis B virus sequences. J Virol 49: 782-792.
56. Borel C, Schorr O, Durand I, Zoulim F, Kay A, et al. (2001) Initial amplification of duck hepatitis B virus covalently closed circular DNA after in vitro infection of embryonic duck hepatocytes is increased by cell cycle progression. Hepatology 34: 168-179.
57. Saade F, Buronfosse T, Pradat P, Abdul F, Cova L, (2008) Enhancement of neutralizing humoral response of DNA vaccine against duck hepatitis B virus envelope protein by co-delivery of cytokine genes. Vaccine 26: 5159-5164.
58. Villet S, Billioud G, Pichoud C, Lucifora J, Hantz O, et al. (2009) In vitro characterization of viral fitness of therapy-resistant hepatitis B variants. Gastroenterology 136: 168-176 e162.
59. Chassot S, Lambert V, Kay A, Godinot C, Roux B, et al. (1993) Fine mapping of neutralization epitopes on duck hepatitis B virus (DHBV) pre-S protein using monoclonal antibodies and overlapping peptides. Virology 192: 217-223.
60. Thermet A, Robaczewska M, Rollier C, Hantz O, Trepo C, et al. (2004) Identification of antigenic regions of duck hepatitis B virus core protein with antibodies elicited by DNA immunization and chronic infection. J Virol 78: 1945-1953.
61. Guo JT, Pugh JC, (1997) Monoclonal antibodies to a 55-kilodalton protein present in duck liver inhibit infection of primary duck hepatocytes with duck hepatitis B virus. J Virol 71: 4829-4831.
62. Narayan R, Buronfosse T, Schultz U, Chevallier-Gueyron P, Guerret S, et al. (2006) Rise in gamma interferon expression during resolution of duck hepatitis B virus infection. J Gen Virol 87: 3225-3232.
63. Ren S, Nassal M, (2001) Hepatitis B virus (HBV) virion and covalently closed circular DNA formation in primary tupaia hepatocytes and human hepatoma cell lines upon HBV genome transduction with replication-defective adenovirus vectors. J Virol 75: 1104-1116.