Fc receptor-mediated, antibody-dependent enhancement of bacteriophage lambda-mediated gene transfer in mammalian cells

Virology

Volumn 373, Issue 2, 2008, Pages 274-286

  Sapinoro, Ramil ^a   Volcy, Ketna ^a   Rodrigo, W W Shanaka I ^a   Schlesinger, Jacob J ^a   Dewhurst, Stephen ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

Actin; Antibody dependent enhancement; Bacteriophage lambda; CD64; Endocytosis; Fc gamma receptor; Fc RI; Gene transfer; Microtubule; Virus vector

Indexed keywords

BAFILOMYCIN A1; CD16 ANTIGEN; CHLORPROMAZINE; CLATHRIN; ENDOSOME ASSOCIATED PROTEIN 1; FC RECEPTOR; FC RECEPTOR IIA; FC RECEPTOR IIB; LATRUNCULIN A; MONENSIN; NOCODAZOLE; PACLITAXEL; PROTEIN DERIVATIVE; UNCLASSIFIED DRUG; VIRUS VECTOR;

ACIDIFICATION; ACTIN FILAMENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY DEPENDENT ENHANCEMENT; ARTICLE; BACTERIOPHAGE LAMBDA; CELL CULTURE; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; GENE EXPRESSION; GENE TRANSFER; GENETIC ASSOCIATION; IMMUNIZATION; IMMUNOCYTOCHEMISTRY; MAMMAL CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN LOCALIZATION; VIRUS INFECTION;

ACTINS; ANIMALS; ANTIBODIES, VIRAL; BACTERIOPHAGE LAMBDA; BICYCLO COMPOUNDS, HETEROCYCLIC; CAPSID PROTEINS; CELL LINE; CERCOPITHECUS AETHIOPS; CHLORPROMAZINE; COS CELLS; ENDOCYTOSIS; GENE TRANSFER TECHNIQUES; GLYCOPROTEINS; HUMANS; LUCIFERASES; MICE; MICROTUBULES; MODELS, BIOLOGICAL; NOCODAZOLE; PACLITAXEL; RECEPTORS, IGG; RECOMBINANT PROTEINS; THIAZOLIDINES; TRANSDUCTION, GENETIC; TRANSFECTION;

ENTEROBACTERIA PHAGE LAMBDA; EUKARYOTA; MAMMALIA; MUS;

EID: 40849147025     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2007.12.013     Document Type: Article

References (61)

1. Almeida J.D., and Waterson A.P. The morphology of virus-antibody interaction. Adv. Virus Res. 15 (1969) 307-338
2. Berg T., Blomhoff R., Naess L., Tolleshaug H., and Drevon C.A. Monensin inhibits receptor-mediated endocytosis of asialoglycoproteins in rat hepatocytes. Exp. Cell Res. 148 2 (1983) 319-330
3. Bowman E.J., Siebers A., and Altendorf K. Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc. Natl. Acad. Sci. U. S. A. 85 21 (1988) 7972-7976
4. Chen X., Scala G., Quinto I., Liu W., Chun T.W., Justement J.S., Cohen O.J., vanCott T.C., Iwanicki M., Lewis M.G., Greenhouse J., Barry T., Venzon D., and Fauci A.S. Protection of rhesus macaques against disease progression from pathogenic SHIV-89.6PD by vaccination with phage-displayed HIV-1 epitopes. Nat. Med. 7 11 (2001) 1225-1231
5. Clark J.R., and March J.B. Bacteriophage-mediated nucleic acid immunisation. FEMS Immunol. Med. Microbiol. 40 1 (2004) 21-26
6. Daeron M. Fc receptor biology. Annu. Rev. Immunol. 15 (1997) 203-234
7. Davis W., Harrison P.T., Hutchinson M.J., and Allen J.M. Two distinct regions of FC gamma RI initiate separate signalling pathways involved in endocytosis and phagocytosis. EMBO J. 14 3 (1995) 432-441
8. di Marzo Veronese F., Willis A.E., Boyer-Thompson C., Appella E., and Perham R.N. Structural mimicry and enhanced immunogenicity of peptide epitopes displayed on filamentous bacteriophage. The V3 loop of HIV-1 gp120. J. Mol. Biol. 243 2 (1994) 167-172
9. Durrbach A., Louvard D., and Coudrier E. Actin filaments facilitate two steps of endocytosis. J. Cell Sci. 109 Pt 2 (1996) 457-465
10. Eguchi A., Akuta T., Okuyama H., Senda T., Yokoi H., Inokuchi H., Fujita S., Hayakawa T., Takeda K., Hasegawa M., and Nakanishi M. Protein transduction domain of HIV-1 Tat protein promotes efficient delivery of DNA into mammalian cells. J. Biol. Chem. 276 28 (2001) 26204-26210
11. Forestell S.P., Dando J.S., Bohnlein E., and Rigg R.J. Improved detection of replication-competent retrovirus. J. Virol. Methods 60 2 (1996) 171-178
12. Geier M.R., and Merril C.R. Lambda phage transcription in human fibroblasts. Virology 47 3 (1972) 638-643
13. Gotoff R., Tamura M., Janus J., Thompson J., Wright P., and Ennis F.A. Primary influenza A virus infection induces cross-reactive antibodies that enhance uptake of virus into Fc receptor-bearing cells. J. Infect. Dis. 169 1 (1994) 200-203
14. Gruenberg J., Griffiths G., and Howell K.E. Characterization of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle fusion in vitro. J. Cell Biol. 108 4 (1989) 1301-1316
15. Guillon C., Schutten M., Boers P.H., Gruters R.A., and Osterhaus A.D. Antibody-mediated enhancement of human immunodeficiency virus type 1 infectivity is determined by the structure of gp120 and depends on modulation of the gp120-CCR5 interaction. J. Virol. 76 6 (2002) 2827-2834
16. Hajitou A., Trepel M., Lilley C.E., Soghomonyan S., Alauddin M.M., Marini III F.C., Restel B.H., Ozawa M.G., Moya C.A., Rangel R., Sun Y., Zaoui K., Schmidt M., von Kalle C., Weitzman M.D., Gelovani J.G., Pasqualini R., and Arap W. A hybrid vector for ligand-directed tumor targeting and molecular imaging. Cell 125 2 (2006) 385-398
17. Harford J., Wolkoff A.W., Ashwell G., and Klausner R.D. Monensin inhibits intracellular dissociation of asialoglycoproteins from their receptor. J. Cell Biol. 96 6 (1983) 1824-1828
18. Hasegawa S., Hirashima N., and Nakanishi M. Microtubule involvement in the intracellular dynamics for gene transfection mediated by cationic liposomes. Gene Ther. 8 21 (2001) 1669-1673
19. Huang Z.Y., Barreda D.R., Worth R.G., Indik Z.K., Kim M.K., Chien P., and Schreiber A.D. Differential kinase requirements in human and mouse Fc-gamma receptor phagocytosis and endocytosis. J. Leukoc. Biol. 80 6 (2006) 1553-1562
20. Hudson J.B., Misra V., and Mosmann T.R. Cytomegalovirus infectivity: analysis of the phenomenon of centrifugal enhancement of infectivity. Virology 72 1 (1976) 235-243
21. Iankov I.D., Pandey M., Harvey M., Griesmann G.E., Federspiel M.J., and Russell S.J. Immunoglobulin g antibody-mediated enhancement of measles virus infection can bypass the protective antiviral immune response. J. Virol. 80 17 (2006) 8530-8540
22. Indik Z., Kelly C., Chien P., Levinson A.I., and Schreiber A.D. Human Fc gamma RII, in the absence of other Fc gamma receptors, mediates a phagocytic signal. J. Clin. Invest. 88 5 (1991) 1766-1771
23. Irving M.B., Pan O., and Scott J.K. Random-peptide libraries and antigen-fragment libraries for epitope mapping and the development of vaccines and diagnostics. Curr. Opin. Chem. Biol. 5 3 (2001) 314-324
24. Ivanenkov V., Felici F., and Menon A.G. Uptake and intracellular fate of phage display vectors in mammalian cells. Biochim. Biophys. Acta 1448 3 (1999) 450-462
25. Jepson C.D., and March J.B. Bacteriophage lambda is a highly stable DNA vaccine delivery vehicle. Vaccine 22 19 (2004) 2413-2419
26. Kassner P.D., Burg M.A., Baird A., and Larocca D. Genetic selection of phage engineered for receptor-mediated gene transfer to mammalian cells. Biochem. Biophys. Res. Commun. 264 3 (1999) 921-928
27. Lankes H.A., Zanghi C.N., Santos K., Capella C., Duke C.M., and Dewhurst S. In vivo gene delivery and expression by bacteriophage lambda vectors. J. Appl. Microbiol. 102 5 (2007) 1337-1349
28. Larocca D., Kassner P.D., Witte A., Ladner R.C., Pierce G.F., and Baird A. Gene transfer to mammalian cells using genetically targeted filamentous bacteriophage. FASEB J. 13 6 (1999) 727-734
29. Leopold P.L., Wendland R.L., Vincent T., and Crystal R.G. Neutralized adenovirus-immune complexes can mediate effective gene transfer via an Fc receptor-dependent infection pathway. J. Virol. 80 20 (2006) 10237-10247
30. Littaua R., Kurane I., and Ennis F.A. Human IgG Fc receptor II mediates antibody-dependent enhancement of dengue virus infection. J. Immunol. 144 8 (1990) 3183-3186
31. Lowry M.B., Duchemin A.M., Robinson J.M., and Anderson C.L. Functional separation of pseudopod extension and particle internalization during Fc gamma receptor-mediated phagocytosis. J. Exp. Med. 187 2 (1998) 161-176
32. March J.B., Clark J.R., and Jepson C.D. Genetic immunisation against hepatitis B using whole bacteriophage lambda particles. Vaccine 22 13-14 (2004) 1666-1671
33. Mercier S., Rouard H., Delfau-Larue M.H., and Eloit M. Specific antibodies modulate the interactions of adenovirus type 5 with dendritic cells. Virology 322 2 (2004) 308-317
34. Merril C.R., Geier M.R., and Petricciani J.C. Bacterial virus gene expression in human cells. Nature 233 5319 (1971) 398-400
35. Minenkova O.O., Ilyichev A.A., Kishchenko G.P., and Petrenko V.A. Design of specific immunogens using filamentous phage as the carrier. Gene 128 1 (1993) 85-88
36. Mollenhauer H.H., Morre D.J., and Rowe L.D. Alteration of intracellular traffic by monensin; mechanism, specificity and relationship to toxicity. Biochim. Biophys. Acta 1031 2 (1990) 225-246
37. Mu F.T., Callaghan J.M., Steele-Mortimer O., Stenmark H., Parton R.G., Campbell P.L., McCluskey J., Yeo J.P., Tock E.P., and Toh B.H. EEA1, an early endosome-associated protein. EEA1 is a conserved alpha-helical peripheral membrane protein flanked by cysteine "fingers" and contains a calmodulin-binding IQ motif. J. Biol. Chem. 270 22 (1995) 13503-13511
38. O'Doherty U., Swiggard W.J., and Malim M.H. Human immunodeficiency virus type 1 spinoculation enhances infection through virus binding. J. Virol. 74 21 (2000) 10074-10080
39. Odin J.A., Edberg J.C., Painter C.J., Kimberly R.P., and Unkeless J.C. Regulation of phagocytosis and [Ca2+]i flux by distinct regions of an Fc receptor. Science 254 5039 (1991) 1785-1788
40. Parren P.W., and Burton D.R. The antiviral activity of antibodies in vitro and in vivo. Adv. Immunol. 77 (2001) 195-262
41. Peiris J.S., and Porterfield J.S. Antibody-mediated enhancement of Flavivirus replication in macrophage-like cell lines. Nature 282 5738 (1979) 509-511
42. Porterfield J.S. Antibody-mediated enhancement of rabies virus. Nature 290 5807 (1981) 542
43. Ravetch J.V., and Bolland S. IgG Fc receptors. Annu. Rev. Immunol. 19 (2001) 275-290
44. Rodrigo W.W., Jin X., Blackley S.D., Rose R.C., and Schlesinger J.J. Differential enhancement of dengue virus immune complex infectivity mediated by signaling-competent and signaling-incompetent human Fcgamma RIA (CD64) or FcgammaRIIA (CD32). J. Virol. 80 20 (2006) 10128-10138
45. Rosa G.T., Gillet L., Smith C.M., de Lima B.D., and Stevenson P.G. IgG fc receptors provide an alternative infection route for murine gamma-herpesvirus-68. PLoS ONE 2 (2007) e560
46. Rosette C., and Karin M. Cytoskeletal control of gene expression: depolymerization of microtubules activates NF-kappa B. J. Cell Biol. 128 6 (1995) 1111-1119
47. Sathaliyawala T., Rao M., Maclean D.M., Birx D.L., Alving C.R., and Rao V.B. Assembly of human immunodeficiency virus (HIV) antigens on bacteriophage T4: a novel in vitro approach to construct multicomponent HIV vaccines. J. Virol. 80 15 (2006) 7688-7698
48. Schlesinger J.J., and Brandriss M.W. Growth of 17D yellow fever virus in a macrophage-like cell line, U937: role of Fc and viral receptors in antibody-mediated infection. J. Immunol. 127 2 (1981) 659-665
49. Schlesinger J.J., and Chapman S.E. Influence of the human high-affinity IgG receptor FcgammaRI (CD64) on residual infectivity of neutralized dengue virus. Virology 260 1 (1999) 84-88
50. Simonsen A., Lippe R., Christoforidis S., Gaullier J.M., Brech A., Callaghan J., Toh B.H., Murphy C., Zerial M., and Stenmark H. EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature 394 6692 (1998) 494-498
51. Takada A., and Kawaoka Y. Antibody-dependent enhancement of viral infection: molecular mechanisms and in vivo implications. Rev. Med. Virol. 13 6 (2003) 387-398
52. Takeda A., Tuazon C.U., and Ennis F.A. Antibody-enhanced infection by HIV-1 via Fc receptor-mediated entry. Science 242 4878 (1988) 580-583
53. Takeda A., Sweet R.W., and Ennis F.A. Two receptors are required for antibody-dependent enhancement of human immunodeficiency virus type 1 infection: CD4 and Fc gamma R. J. Virol. 64 11 (1990) 5605-5610
54. Tamura M., Webster R.G., and Ennis F.A. Antibodies to HA and NA augment uptake of influenza A viruses into cells via Fc receptor entry. Virology 182 1 (1991) 211-219
55. Tamura M., Webster R.G., and Ennis F.A. Subtype cross-reactive, infection-enhancing antibody responses to influenza A viruses. J. Virol. 68 6 (1994) 3499-3504
56. Van den Herik-Oudijk I.E., Capel P.J., van der Bruggen T., and Van de Winkel J.G. Identification of signaling motifs within human Fc gamma RIIa and Fc gamma RIIb isoforms. Blood 85 8 (1995) 2202-2211
57. van Vugt M.J., Kleijmeer M.J., Keler T., Zeelenberg I., van Dijk M.A., Leusen J.H., Geuze H.J., and van de Winkel J.G. The FcgammaRIa (CD64) ligand binding chain triggers major histocompatibility complex class II antigen presentation independently of its associated FcR gamma-chain. Blood 94 2 (1999) 808-817
58. Wallace M.J., Smith D.W., Broom A.K., Mackenzie J.S., Hall R.A., Shellam G.R., and McMinn P.C. Antibody-dependent enhancement of Murray Valley encephalitis virus virulence in mice. J. Gen. Virol. 84 Pt 7 (2003) 1723-1728
59. Wang L., and MacDonald R.C. Effects of microtubule-depolymerizing agents on the transfection of cultured vascular smooth muscle cells: enhanced expression with free drug and especially with drug-gene lipoplexes. Molec. Ther. 9 5 (2004) 729-737
60. Zanghi C.N., Lankes H.A., Bradel-Tretheway B., Wegman J., and Dewhurst S. A simple method for displaying recalcitrant proteins on the surface of bacteriophage lambda. Nucleic Acids Res. 33 18 (2005) e160
61. Zanghi C.N., Sapinoro R., Bradel-Tretheway B., and Dewhurst S. A tractable method for simultaneous modifications to the head and tail of bacteriophage lambda and its application to enhancing phage-mediated gene delivery. Nucleic Acids Res. 35 8 (2007) e59