Immobilized HIV-1 Tat protein promotes gene transfer via a transactivation-independent mechanism which requires binding of Tat to viral particles

Journal of Gene Medicine

Volumn 11, Issue 11, 2009, Pages 955-965

  Nappi, Filomena ^a   Chiozzini, Chiara ^a   Bordignon, Valentina ^a,f   Borsetti, Alessandra ^a   Bellino, Stefania ^a   Cippitelli, Marco ^b,c   Barillari, Giovanni ^a   Caputo, Antonella ^d   Tyagi, Mudit ^e,g   Giacca, Mauro ^e   Ensoli, Barbara ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^d UNIVERSITY OF PADOVA   (Italy)

^e INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^f SAN GALLICANO DERMATOLOGICAL INSTITUTE   (Italy)

^g CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

Gene therapy; Immobilized virus; Tat; Viral transduction

Indexed keywords

CD4 ANTIGEN; CHLORAMPHENICOL ACETYLTRANSFERASE; GREEN FLUORESCENT PROTEIN; LENTIVIRUS VECTOR; RETROVIRUS VECTOR; TRANSACTIVATOR PROTEIN; VIRUS ENVELOPE PROTEIN;

ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; PRIORITY JOURNAL; REPORTER GENE; TRANSACTIVATION; VESICULAR STOMATITIS VIRUS; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; VIRUS ATTACHMENT; VIRUS MUTANT; VIRUS PARTICLE; VIRUS RECOMBINANT;

BINDING SITES; RECOMBINANT PROTEINS; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; TRANSCRIPTIONAL ACTIVATION; TRANSDUCTION, GENETIC; VIRION; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1; LENTIVIRUS; VESICULAR STOMATITIS VIRUS;

EID: 72949119184     PISSN: 1099498X     EISSN: 15212254     Source Type: Journal    
DOI: 10.1002/jgm.1381     Document Type: Article

References (49)

1. Hanenberg H, Xiao XL, Dilloo D, et al. Colocalization of retrovirus and target cells on specific fibronectin fragments increases genetic transduction of mammalian cells. Nat Med 1996; 2: 876-882.
2. Moritz T, Dutt P, Xiao X, et al. Fibronectin improves transduction of reconstituting hematopoietic stem cells by retroviral vectors: evidence of direct viral binding to chymotryptic carboxy-terminal fragments. Blood 1996; 88: 855-862.
3. Pollok KE, Williams DA. Facilitation of retrovirus-mediated gene transfer into hematopoietic stem and progenitor cells and peripheral blood T-lymphocytes utilizing recombinant fibronectin fragments. Curr Opin Mol Ther 1999; 1: 595-604.
4. Arya SK, Guo C, Josephs SF, Wong-Staal F. Trans-activator gene of human T-lymphotropic virus type III (HTLV-III). Science 1985; 229: 69-73.
5. Cullen BR, Greene WC. Regulatory pathways governing HIV-1 replication. Cell 1989; 58: 423-426.
6. Fisher AG, Feinberg MB, Josephs SF, et al. The trans-activator gene of HTLV-III is essential for virus replication. Nature 1986; 320: 367-371.
7. Sodroski J, Patarca R, Rosen C, Wong-Staal F, Haseltine W. Location of the trans-activating region on the genome of human T-cell lymphotropic virus type III. Science 1985; 229: 74-77.
8. Wu Y, Marsh JW. Selective transcription and modulation of resting T cell activity by preintegrated HIV DNA. Science 2001; 293: 1503-1506.
9. Betti M, Voltan R, Marchisio M, et al. Characterization of HIV-1 Tat proteins mutated in the transactivation domain for prophylactic and therapeutic application. Vaccine 2001; 19: 3408-3419.
10. Chang HC, Samaniego F, Nair BC, Buonaguro L, Ensoli B. HIV-1 Tat protein exits from cells via a leaderless secretory pathway and binds to extracellular matrix-associated heparan sulfate proteoglycans through its basic region. Aids 1997; 11: 1421-1431.
11. Ensoli B, Barillari G, Salahuddin SZ, Gallo RC, Wong-Staal F. Tat protein of HIV-1 stimulates growth of cells derived from Kaposi's sarcoma lesions of AIDS patients. Nature 1990; 345: 84-86.
12. Ensoli B, Buonaguro L, Barillari G, et al. Release, uptake, and effects of extracellular human immunodeficiency virus type 1 Tat protein on cell growth and viral transactivation. J Virol 1993; 67: 277-287.
13. Tyagi M, Rusnati M, Presta M, Giacca M. Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans. J Biol Chem 2001; 276: 3254-3261.
14. Ensoli B, Gendelman R, Markham P, et al. Synergy between basic fibroblast growth factor and HIV-1 Tat protein in induction of Kaposi's sarcoma. Nature 1994; 371: 674-680.
15. Ensoli B, Sgadari C, Barillari G, et al. Biology of Kaposi's sarcoma. Eur J Cancer 2001; 37: 1251-1269.
16. Westendorp MO, Frank R, Ochsenbauer C, et al. Sensitization of T cells to CD95-mediated apoptosis by HIV-1 Tat and gp120. Nature 1995; 375: 497-500.
17. Wieland U, Kuhn JE, Jassoy C, et al. Antibodies to recombinant HIV-1 vif, tat, and nef proteins in human sera. Med Microbiol Immunol (Berl) 1990; 179: 1-11.
18. Xiao H, Neuveut C, Tiffany HL, et al. Selective CXCR4 antagonism by Tat: implications for in vivo expansion of coreceptor use by HIV-1. Proc Natl Acad Sci USA 2000; 97: 11466-11471.
19. Fawell S, Seery J, Daikh Y, et al. Tat-mediated delivery of heterologous proteins into cells. Proc Natl Acad Sci USA 1994; 91: 664-668.
20. Frankel AD, Pabo CO. Cellular uptake of the tat protein from human immunodeficiency virus. Cell 1988; 55: 1189-1193.
21. de Paulis A, De Palma R, Di Gioia L, et al. Tat protein is an HIV-1-encoded beta-chemokine homolog that promotes migration and up-regulates CCR3 expression on human Fc epsilon RI+ cells. J Immunol 2000; 165: 7171-7179.
22. Huang L, Bosch I, Hofmann W, Sodroski J, Pardee AB. Tat protein induces human immunodeficiency virus type 1 (HIV-1) coreceptors and promotes infection with both macrophagetropic and T-lymphotropic HIV-1 strains. J Virol 1998; 72: 8952-8960.
23. Secchiero P, Zella D, Capitani S, Gallo RC, Zauli G. Extracellular HIV-1 tat protein up-regulates the expression of surface CXCchemokine receptor 4 in resting CD4+ T cells. J Immunol 1999; 162: 2427-2431.
24. Weiss JM, Nath A, Major EO, Berman JW. HIV-1 Tat induces monocyte chemoattractant protein-1-mediated monocyte transmigration across a model of the human blood-brain barrier and up-regulates CCR5 expression on human monocytes. J Immunol 1999; 163: 2953-2959.
25. Barillari G, Gendelman R, Gallo RC, Ensoli B. The Tat protein of human immunodeficiency virus type 1, a growth factor for AIDS Kaposi sarcoma and cytokine-activated vascular cells, induces adhesion of the same cell types by using integrin receptors recognizing the RGD amino acid sequence. Proc Natl Acad Sci USA 1993; 90: 7941-7945.
26. Barillari G, Sgadari C, Fiorelli V, et al. The Tat protein of human immunodeficiency virus type-1 promotes vascular cell growth and locomotion by engaging the alpha5beta1 and alphavbeta3 integrins and by mobilizing sequestered basic fibroblast growth factor. Blood 1999; 94: 663-672.
27. Barillari G, Ensoli B. Angiogenic effects of extracellular human immunodeficiency virus type 1 Tat protein and its role in the pathogenesis of AIDS-associated Kaposi's sarcoma. Clin Microbiol Rev 2002; 15: 310-326.
28. Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC. Green fluorescent protein as a marker for gene expression. Science 1994; 263: 802-805.
29. Graham FL, Smiley J, Russell WC, Nairn R. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J Gen Virol 1977; 36: 59-74.
30. Felber BK, Hadzopoulou-Cladaras M, Cladaras C, Copeland T, Pavlakis GN. rev protein of human immunodeficiency virus type 1 affects the stability and transport of the viral mRNA. Proc Natl Acad Sci USA 1989; 86: 1495-1499.
31. Graham FL, van der Eb AJ. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology 1973; 52: 456-467.
32. Yu X, Zhan X, D'Costa J, et al. Lentiviral vectors with two independent internal promoters transfer high-level expression of multiple transgenes to human hematopoietic stem-progenitor cells. Mol Ther 2003; 7: 827-838.
33. Soneoka Y, Cannon PM, Ramsdale EE, et al. A transient threeplasmid expression system for the production of high titer retroviral vectors. Nucleic Acids Res 1995; 23: 628-633.
34. Mochizuki H, Schwartz JP, Tanaka K, Brady RO, Reiser J. Hightiter human immunodeficiency virus type 1-based vector systems for gene delivery into nondividing cells. J Virol 1998; 72: 8873-8883.
35. Naldini L, Blomer U, Gallay P, et al. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 1996; 272: 263-267.
36. Helseth E, Kowalski M, Gabuzda D, et al. Rapid complementation assays measuring replicative potential of human immunodeficiency virus type 1 envelope glycoprotein mutants. J Virol 1990; 64: 2416-2420.
37. Rossi GB, Verani P, Macchi B, et al. Recovery of HIV-related retroviruses from Italian patients with AIDS or AIDS-related complex and from asymptomatic at-risk individuals. Ann NY Acad Sci 1987; 511: 390-400.
38. Fanales-Belasio E, Moretti S, Nappi F, et al. Native HIV-1 Tat protein targets monocyte-derived dendritic cells and enhances their maturation, function, and antigen-specific T cell responses. J Immunol 2002; 168: 197-206.
39. Demarchi F, Gutierrez MI, Giacca M. Human immunodeficiency virus type 1 tat protein activates transcription factor NF-kappaB through the cellular interferon-inducible, double-stranded RNAdependent protein kinase, PKR. J Virol 1999; 73: 7080-7086.
40. Mitola S, Soldi R, Zanon I, et al. Identification of specific molecular structures of human immunodeficiency virus type 1 Tat relevant for its biological effects on vascular endothelial cells. J Virol 2000; 74: 344-353.
41. Liao Z, Roos JW, Hildreth JE. Increased infectivity of HIV type 1 particles bound to cell surface and solid-phase ICAM-1 and VCAM-1 through acquired adhesionmolecules LFA-1 and VLA-4. AIDS Res Hum Retroviruses 2000; 16: 355-366.
42. Greco G, Pal S, Pasqualini R, Schnapp LM. Matrix fibronectin increases HIV stability and infectivity. J Immunol 2002; 168: 5722-5729.
43. Sandrin V, Boson B, Salmon P, et al. Lentiviral vectors pseudotyped with a modified RD114 envelope glycoprotein show increased stability in sera and augmented transduction of primary lymphocytes and CD34+ cells derived from human and nonhuman primates. Blood 2002; 100: 823-832.
44. Tellier MC, Greco G, Klotman M, et al. Superfibronectin, a multimeric form of fibronectin, increases HIV infection of primary CD4+ T lymphocytes. J Immunol 2000; 164: 3236-3245.
45. Lei P, Bajaj B, Andreadis ST. Retrovirus-associated heparan sulfate mediates immobilization and gene transfer on recombinant fibronectin. J Virol 2002; 76: 8722-8728.
46. Marchio S, Alfano M, Primo L, et al. Cell surface-associated Tat modulates HIV-1 infection and spreading through a specific interaction with gp120 viral envelope protein. Blood 2005; 105: 2802-2811.
47. Albini A, Soldi R, Giunciuglio D, et al. The angiogenesis induced by HIV-1 tat protein is mediated by the Flk-1/KDR receptor on vascular endothelial cells. Nat Med 1996; 2: 1371-1375.
48. Albini A, Ferrini S, Benelli R, et al. HIV-1 Tat protein mimicry of chemokines. Proc Natl Acad Sci USA 1998; 95: 13153-13158.
49. Hennemann B, Chuo JY, Schley PD, et al. High-efficiency retroviral transduction of mammalian cells on positively charged surfaces. Hum Gene Ther 2000; 11: 43-51.