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

Volumn 11, Issue 12, 1997, Pages 1421-1431

  Chang, Hsiao C ^a   Samaniego, Felipe ^a,b   Nair, Bala C ^c   Buonaguro, Luigi ^a,d   Ensoli, Barbara ^a,e  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF MARYLAND GREENEBAUM CANCER CENTER   (United States)

^c ADVANCED BIOSCIENCE LABORATORIES INC   (United States)

^d NATIONAL CANCER INSTITUTE   (Italy)

^e ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

AIDS; Extracellular; Heparin binding; Kaposi's sarcoma; Proteoglycans; Release; Tat

Indexed keywords

PROTEOHEPARAN SULFATE; TRANSACTIVATOR PROTEIN;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; AFFINITY CHROMATOGRAPHY; ANIMAL CELL; ARTICLE; BLOOD LEVEL; CELL STRAIN COS1; CONTROLLED STUDY; EXTRACELLULAR MATRIX; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROVIRUS; TEMPERATURE; VIRUS CELL INTERACTION;

EID: 0030862924     PISSN: 02699370     EISSN: None     Source Type: Journal    
DOI: 10.1097/00002030-199712000-00006     Document Type: Article

References (64)

1. Arya SK, Guo C, Josephs SF, Wong-Staal F: Transactivator gene of human T-lymphotropic virus type III (HTLV-III). Science I985, 229:69-73.
2. Dayton AI, Sodroski JG, Rosen CA, Goh WC, Haseltine WA: The trans-activator gene of the human T-cell lymphotropic virus type III is required for replication. Cell 1986, 44:941-947.
3. fisher AG, Foinberg MB, Josephs SF, et al.: The trans-activator gene of HTLV-III is essential for virus replication. Nature 1986, 320:367-371.
4. Sodroski JG, Patarca R, Rosen CA. Wong-Staal F, Haseltine WA: Location of the trans-activating region on the genome of human T-cell lymphotropic virus type III. Science 1985, 229:74-77
5. Chang HK, Gallo RC, Ensoli B: Regulation of cellular gene expression and function by the human immunodeficiency virus type 1 Tat protein. J Biomed Sci 1995, 2:189-202.
6. Caputo A, Grossi MP, Rossi C, et al.: The tat gene and protein of the human immunodeficiency virus type 1. Microbiologica 1995, 18:87-110.
7. Brake DA, Debouck C, Bieseeker G: Identification of an ArgGly-Asp (RGD) cell adhesion site in human immunodeficiency virus type 1 transactivation protein, Tat. J Cell Biol 1990, 111:1275-1281.
8. Vogel BE, Eee SJ, Hieldebrand A, et al.: A novel integrin specificity exemplified by binding of the avβ5 integrin to the basic domain of the HIV-1 Tat protein and vitronectin. J Cell Biol 1993, 121:461-468.
9. 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 sequence, Proc Natl Acad Sci USA 1993, 90:7941-7945.
10. 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.
11. Zauli G, Gibellini D, Celeghini C, et al.: Pleiotropic effects of immobilized versus soluble recombinant HIV-1 Tat protein on CD3-mediated activation, induction of apoptosis, and HIV-1 LTR transactivation in purified CD4+ T lymphocytes. J Immunol 1996, 157:2216-2274
12. Vogol I, Hinrichs SH, Reynolds RK, Luciw PA, lay G: The HIV tat gene induces dermal lesions resembling Kaposi's sarcoma in transgenic mice. Nature 1988, 335:606-611.
13. Corallini A, Altavilla G, Pozzi L, et al.: Systemic expression of HIV-1 tet gene in transgenic mice induces endothelial proliferation and tumors of different histotypes. Cancer Res 1993, 53:5569-5575.
14. Frankel AD, Pabo CO: Cellular uptake of the Tat protein from human immunodeficiency virus. Cell 1988 55:1189-1193.
15. Helland DC, Welles JL, Caputo A, Haseltine WA: Transcellular transactivation by the human immunodeficiency virus type 1 Tat protein. J Virol 1991, 65:4547-4549.
16. Feinberg MB, Baltimore D, Frankel AD: The role of Tat in the human immunodeficiency virus life cycle indicates a primary effect on transcriptional elongation. Proc Natl Acad Sci USA 1991, 88:4045-4049.
17. Marcuzzi A, Weinberger J, Weinberger OK: Transcellular activation of the human immunodeficiency virus type 1 long terminal repeat in cocultured lymphocytes. J Virol 1992, 66:4228-4232.
18. Ensoli B, Buanaguro 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 1991, 67:277-287.
19. Re MC, Furlini G, Vignoli M, et al.: Effect of antibody to HIV-1 Tat protein on viral and progression of HIV-1 disease in vivo. J Acquir Immune Detic Syndr Hum Retrovirus 1995, 10:408-412.
20. Albini A, Barillari Ci, Benelli R, Gallo RC, Ensoli B: Angiogenic properties of human immunodeficiency virus type 1 Tat protein. Proc Natl Acad Sci USA 1995, 92:4838-4842.
21. Albini A, Benelli R, Presta M, Rusnati M, et al.: HIV-1 Tat protein is a heparin binding angiogenic growth factor. Ongogene 1996, 12:289-297.
22. Barillari G, Buonaguro L, Fiorelli V, et al.: Effects of cytokines from activated immune cells on vascular cell growth and HIV-1 gene expression: implications for AIDS-Kaposi's sarcoma pathogenesis. J Immunol 1992, 149: 3727-3734.
23. Ensoli B, Barillari G, Salahuddin SZ, Gallo RC, Wong-Saal F: Tat protein of HIV-1 stimulates growth of cells derived from Kaposi's sarcoma lesions of AIDS patients. Nature 1990 345:84-86.
24. Fiorelli V, Gendelman R, Samaniego F, Markham PD, Ensoli B: Cytokines from activated T cells induce normal endothelial cells to acquire the phenotypic and functional features of AIDS-Kaposi's sarcoma spindle cells. J Clin Invest 1995, 95:1723-1734.
25. Albini A, Fontanini G, Masiello L, et al.: Angiogenic potential in vivo by Kaposi's sarcoma cell-free supernatants and HIV-1 tat product: inhibition of KS-like lesions by tissue inhibitor of metalloproteinase-2. AIDS 1994, 8:1237-1244.
26. Li CJ, Friedman DJ, Wang C, Metelev V, Pardee AB: Induction of apoptosis in uninfected lymphocytes by HIV-1 Tat protein. Science 1995, 268:429-431.
27. Westendorp MO, Shatrov VA, Schulze-Osthoff K, et al.: HIV-1 Tat potentiates TNF-induced NF-kB activation and cytotoxicity by altering the cellular redox state. EMBO J 1995, 14:546-554.
28. 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.
29. Caputo A, Sodroski JG, Haseltine WA: Constitutive expression of HIV-1 Tat protein in human Jurkat T cells using a BK virus vector. J Acquir Immune Defic Syndr 1990, 3:372-379.
30. Zauli G, Gihellini D, Milani D, et al.: Human immunodeficiency virus type 1 Tat protein protects lymphoid, epithelial, and neuronal cell lines from death by apoptosis. Cancer Res 1993, 53:4481-4485.
31. Gibellini D, Caputo A, Celeghini C, et al.: Tat-expressing Jurkat cells show an increased resistance to different apoptotic stimuli, including acute human immunodeficiency virus-type 1 (HIV-1) infection. Br J Haematol 1995, 89:24-33.
32. Fawell S, Seery I, Daikh Y, et al.: Tat-mediated delivery of heterologous proteins into cells. Proc Natl Acad Sci USA 1994, 91:664-668.
33. Anderson DC, Nichols E, Manger R, Woodle D, Barry M, Fritzberg AR: Tumor cell retention of antibody Fab fragments is enhanced by an attached HIV Tat protein-derived peptide. Hiochem Biaphys Res Commun 1993, 194:876-884.
34. Pepinsky KB, Androphy EJ, Corina K, Barsoum J: Specific inhibition of a human papillomavirus E2 trans-activator by intracellular delivery of its repressor. DNA Cell Biol 1994, 13:1011-1019.
35. Rubartelli A, Cozzolino F, Talio M, Sitia R: A novel secretory pathway for interleukin-1β, a protein lacking a signal sequence. EMBO J 1990, 9:1505-1510.
36. !6. Cooper DNW, Barondes SH: Evidence for export of a muscle lectin from cytosol to extracellular matrix and a novel secretion mechanism. J Cell Biol 1990, 110:1681-1691.
37. \7. Jackson A, Friedman S, Zhan X, Engleka KA, Foreman R, Maciag T: Heat shock induces the release of fibroblast growth factor 1 from NIH 3T3 cells. Proc Natl Acad Sci USA 1992, 89:10691-10695.
38. Jackson A, Tarantini F, Gamble S, Friedman S, Maciag T: The release of fibroblast growth factor-1 from NIH 3T3 cells in response to temperature involves the function of cysteine residues. J Biol Chem 1995, 270:33-36.
39. Mignatti P, Morimoto T, Rifkin DB: Basic fibroblast growth factor, a protein devoid of secretory signal sequence, is released by cells via a pathway independent of the endoplasmic reticulum-Golgi complex. J Cell Physiol 1992, 151:81-93.
40. Samaniego, F, Markham PD, Gallo RC, Ensoli B: Inflammatory cytokines induce AIDS-Kaposi's sarcoma-derived spindle cells to produce and release basic fibroblast growth factor and enhance Kaposi's sarcoma-like lesion formation in nude mice. J Immunol 1995, 154:3582-3592.
41. Samaniego F, Markham PD, Gendelman R, Gallo RC, Ensoli B: Inflammatory cytokines induce endothelial cells to produce and release basic fibroblast growth factor and to promote Kaposi's sarcoma-like lesions in nude mice. J Immunol 1997, 158:1887-1894.
42. Rubartelli A, Bajetto A, Allavena G, Wollman E, Sitia R: Secretion of thioredoxin by normal and neoplastic cells through a leaderless secretory pathway. J Biol Chem 1992, 267:24161-24164.
43. Sadaie MR, Tschachler E, Valerie K, et al.: Activation of Tatdefective human immunodeficiency virus by ultraviolet light. New Biol 1990, 2:479-486.
44. Bohan CA, Kashanchi F, Ensoli B, Buonaguro L, Brady J: Analysis of Tat transactivation of human immunodeficiency virus transcription in vitro. Gene Expr 1992, 2:391-407.
45. Misumi Y, Miki K, Takatsushi A, Tanuira G, Ikehara Y: Novel blockade by brefeldin A of intracellular transport of secretory proteins in cultured rat hepatocytes. J Biol Chem 1986, 261:1398-11401.
46. 2-macroglobulin and EGF on the fibroblast cell surface. Nature 1979, 277:661-663.
47. Mann DA, Frankel AD: Endocytosis and targeting of exogenous HIV-1 Tat protein. EMBO J 1991, 10:1733-1739.
48. Saksela O, Mostatelli D, Sommer A, Rifkin DB: Endothelial cellderived heparan sulfate binds basic fibroblast growth factor and protects it from proteolytic degradation. J Cell Biol 1988, 107:743-751.
49. Hassell JR, Kimura JH, Hastall VC: Proteoglycan core protein families. Annu Rev Biochem 1986, 55:539-567.
50. Cospodarowitz D, Chang J: Heparin protects basic and acidic FGF from inactivation. J Cell Physiol 1986, 128:475-484.
51. Esch F, Baird A, Ling N, et al.: Primary structure of bovine pituitary basic fibroblast growth factor (FCF) and comparison with the amino-terminal sequence of bovine brain acidic FGF. Proc Natl Acad Sci USA 1985, 85:6507-6511.
52. Baird A, Schubert D, Ling N, Guilleniin R: Receptor- and heparin-binding domains of basic fibroblast growth factor. Proc Natl Acad Sci USA 1988, 85:2324-2328.
53. Raines EW, ROSS R: Compartmentalization of PDGF on extracellular binding sites dependent on exon 6 encoded sequences. J Cell Biol 1992, 116:533-543.
54. Ruoslahti E: Fibronectin and its receptors. Annu Rev Biochem 1988, 57:375-411.
55. Frankel AD, Bredt D, Pabo C: Tat protein from immunodeficiency virus forms a metal-linked dimer. Science 1988, 240:70-73.
56. Tarantini F, Gamble S, Jackson A, Matiag T: The cysteine residue responsible for the release of fibroblast growth factor-1 resides in a domain independent of the domain for phosphatidylserine binding. J Biol Chem 1995, 270:29039-29042.
57. Marcum JA, Atha DH, Fritze LMS, Nawroth P, Stern D, Rosenberg RD: Cloned bovine aortic endothelial cells synthesize anticoagulantly active heparan sulfate proteoglycan. J Biol Chem 1986, 261:7507-7517.
58. Dingwall C, Ernberg I, Gait MJ, et al.: HIV-1 Tat protein stimulates transcription by binding to a U-rich bulge in the stem of the TAR RNA structure. EMBO J 1990, 9:4145-4153.
59. Muller WEG, Okamoto T, Reuter P, Ugarkovit D, Schroder HC: Functional characterization of Tat protein from human immunodeficiency virus. Evidence that Tat links viral RNAs to nuclear matrix. J Biol Chem 1990, 265:3803-3808.
60. Stamaloglou SC, Keller JM: Correlation between cell substrate attachment in vitro and cell surface heparan sulfate affinity for fibronectin and collagen. J Cell Biol 1983, 96:1820-1823.
61. Isemura M, Sato N, Yamaguchi Y, et al.: Isolation and characterization of fibronectin-binding proteoglycan carrying both heparan sulfate and dermatan sulfate chains from human placenta. J Biol Chem 1987, 262:8926-8933.
62. Carey DJ, Rafferly CM, Schramm MM: Association of heparan sulfate proteoglycan and laminin with the cytoskeleton in rat liver. J Biol Chem 1987, 262:3376-3381.
63. Chang HK, Gendelman R, Lisziewicz I, Gallo RC, Ensoli B: Block of HIV-1 infection by a combination of antisense tat RNA and TAR decoys: a strategy for control of HIV-1. Gene Ther 1994, 1:208-216.
64. Goldstein G: HIV-1 Tat protein as a potential AIDS vaccine. Nature Med 1996, 9:960-964.