HIV-1 Tat reprograms immature dendritic cells to express chemoattractants for activated T cells and macrophages

Nature Medicine

Volumn 9, Issue 2, 2003, Pages 191-197

  Izmailova, Elena ^a   Bertley, Frederic M N ^a   Huang, Qian ^b   Makori, Norbert ^c   Miller, Christopher J ^c,d   Young, Richard A ^b,e   Aldovini, Anna ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOATTRACTANT; CHEMOKINE; GENE PRODUCT; INTERFERON; MONOCYTE CHEMOTACTIC PROTEIN 2; TRANSACTIVATOR PROTEIN;

ADOLESCENT; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; CELL ACTIVATION; CELL MATURATION; CHEMOTAXIS; DENDRITIC CELL; DNA MICROARRAY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MACACA; MACROPHAGE; MONKEY DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETROVIRUS INFECTION; SIMIAN IMMUNODEFICIENCY VIRUS; T LYMPHOCYTE;

ANIMALS; CHEMOTAXIS, LEUKOCYTE; DENDRITIC CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, VIRAL; GENE PRODUCTS, TAT; HIV-1; HUMANS; INTERFERONS; LYMPHOCYTE ACTIVATION; MACACA; MACROPHAGES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES; UP-REGULATION;

ANIMALIA; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; MACACA; SIMIAE; SIMIAN IMMUNODEFICIENCY VIRUS; UNIDENTIFIED RETROVIRUS;

EID: 0037330043     PISSN: 10788956     EISSN: None     Source Type: Journal    
DOI: 10.1038/nm822     Document Type: Article

References (45)

1. Stahl-Hennig, C. et al. Rapid infection of oral mucosal-associated lymphoid tissue with simian immunodeficiency virus. Science 285, 1261-1265 (1999).
2. + T cells. Science 286, 1353-1357 (1999).
3. Granelli-Piperno, A., Delgado, E., Finkel, V., Paxton, W. & Steinman, R.M. Immature dendritic cells selectively replicate macrophagetropic (M-tropic) human immunodeficiency virus type 1, while mature cells efficiently transmit both M- and T-tropic virus to T cells. J. Virol. 72, 2733-2737 (1998).
4. Hu, J., Gardner, M.B. & Miller, C.J. Simian immunodeficiency virus rapidly penetrates the cervicovaginal mucosa after intravaginal inoculation and infects intraepithelial dendritic cells. J. Virol. 74, 6087-6095 (2000).
5. Rescigno, M. et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol. 2, 361-367 (2001).
6. Geijtenbeek, T.B. et al. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100, 587-597 (2000).
7. Banchereau, J. et al. Immunobiology of dendritic cells. Annu. Rev. Immunol. 18, 767-811 (2000).
8. Mellman, I. & Steinman, R.M. Dendritic cells: specialized and regulated antigen processing machines. Cell 106, 255-258 (2001).
9. Huang, Q. et al. The plasticity of dendritic cell responses to pathogens and their components. Science 294, 870-875 (2001).
10. Tortorella, D., Gewurz, B.E., Furman, M.H., Schust, D.J. & Ploegh, H.L. Viral subversion of the immune system. Annu. Rev. Immunol. 18, 861-926 (2000).
11. Engelmayer, J. et al. Vaccinia virus inhibits the maturation of human dendritic cells: a novel mechanism of immune evasion. J. Immunol. 163, 6762-6768 (1999).
12. + T cells. J. Exp. Med. 186, 801-812 (1997).
13. de Noronha, C.M. et al. Dynamic disruptions in nuclear envelope architecture and integrity induced by HIV-1 Vpr. Science 294, 1105-1108 (2001).
14. Viscidi, R.P., Mayur, K., Lederman, H.M. & Frankel, A.D. Inhibition of antigen-induced lymphocyte proliferation by Tat protein from HIV-1. Science 246, 1606-1608 (1989).
15. New, D.R., Ma, M., Epstein, L.G., Nath, A. & Gelbard, H.A. Human immunodeficiency virus type 1 Tat protein induces death by apoptosis in primary human neuron cultures. J. Neurovirol. 3, 168-173 (1997).
16. Swingler, S. et al. HIV-1 Nef mediates lymphocyte chemotaxis and activation by infected macrophages. Nature Med. 5, 997-1103 (1999).
17. Simmons, A., Aluvihare, V. & McMichael, A. Nef triggers a transcriptional program in T cells imitating single-signal T cell activation and inducing HIV virulence mediators. Immunity 14, 763-777 (2001).
18. Messner, D. et al. Endogenously expressed nef uncouples cytokine and chemokine prouction from membrane phenotypic maturation in dendritic cells. J. Immunol. 169, 4172-4182 (2002).
19. Wu, Y. & Marsh, J.W. Selective transcription and modulation of resting T cell activity by preintegrated HIV DNA. Science 293, 1503-1506 (2001).
20. Jones, K.A. Taking a new TAK on tat transactivation. Genes Dev. 11, 2593-2599 (1997).
21. Demarchi, F., Gutierrez, M.I. & Giacca, M. Human immunodeficiency virus type 1 tat protein activates transcription factor NF-κB through the cellular interferon-inducible, double-stranded RNA-dependent protein kinase, PKR. J. Virol. 73, 7080-7086 (1999).
22. Marzio, G. & Giacca, M. Chromatin control of HIV-1 gene expression. Genetica 106, 125-130 (1999).
23. Chartier, C. et al. Efficient generation of recombinant adenovirus vectors by homologous recombination in Escherichia coli. J. Virol. 70, 4805-4810 (1996).
24. Zhang, L. & Pagano, J.S. Review: structure and function of IRF-7. J. Interferon Cytokine Res. 22, 95-101 (2002).
25. Ramana, C.V., Gil, M.P., Schreiber, R.D. & Stark, G.R. Stat1-dependent and -independent pathways in IFN-γ-dependent signaling. Trends Immunol. 23, 96-101 (2002).
26. Bazan, J.F. et al. A new class of membrane-bound chemokine with a CX3C motif. Nature 385, 640-644 (1997).
27. Luster, A.D., Unkeless, J.C. & Ravetch, J.V. γ-interferon transcriptionally regulates an early-response gene containing homology to platelet proteins. Nature 315, 672-676 (1985).
28. Piali, L. et al. The chemokine receptor CXCR3 mediates rapid and shear-resistant adhesion-induction of effector T lymphocytes by the chemokines IP10 and Mig. Eur. J. Immunol. 28, 961-972 (1998).
29. Van Damme, J., Proost, P., Lenaerts, J.P. & Opdenakker, G. Structural and functional identification of two human, tumor-derived monocyte chemotactic proteins (MCP-2 and MCP-3) belonging to the chemokine family. J. Exp. Med. 176, 59-65 (1992).
30. Wu, L. et al. Rhesus macaque dendritic cells efficiently transmit primate lentiviruses independently of DC-SIGN. Proc. Natl. Acad. Sci. USA 99, 1568-1573 (2002).
31. Smith, S.G., Patel, P.M., Selby, P.J. & Jackson, A.M. The response of human dendritic cells to recombinant adenovirus, recombinant Mycobacterium bovis Bacillus Calmette Guerin and biolistic methods of antigen delivery: different induction of contact-dependant and soluble signals. Immunol. Lett. 76, 79-88 (2001).
32. + T cells. Nature 417, 95-98 (2002).
33. + T cells in the lungs of patients with HIV infection and T-cell alveolitis. Am. J. Respir. Crit. Care Med. 162, 1466-1473 (2000).
34. Frankel, A.D. & Pabo, C.O. Cellular uptake of the tat protein from human immunodeficiency virus. Cell 55, 1189-1193 (1988).
35. Sen, G.C. Novel functions of interferon-induced proteins. Semin. Cancer Biol. 10, 93-101 (2000).
36. Chang, Y.E. & Laimins, L.A. Microarray analysis identifies interferon-inducible genes and Stat-1 as major transcriptional targets of human papillomavirus type 31. J. Virol. 74, 4174-4182 (2000).
37. Fujii, N., Yokosawa, N. & Shirakawa, S. Suppression of interferon response gene expression in cells persistently infected with mumps virus, and restoration from its suppression by treatment with ribavirin. Virus Res. 65, 175-185 (1999).
38. Weihua, X. et al. The polyoma virus T antigen interferes with interferon-inducible gene expression. Proc. Natl. Acad. Sci. USA 95, 1085-1090 (1998).
39. + T cells in HIV-1-infected hu-PBL-NOD-SCID mice. J. Exp. Med. 193, 651-660 (2001).
40. Katsikis, P.D. et al. Interleukin-1 beta converting enzyme-like protease involvement in Fas-induced and activation-induced peripheral blood T cell apoptosis in HIV infection. TNF-related apoptosis-inducing ligand can mediate activation-induced T cell death in HIV infection. J. Exp. Med. 186, 1365-1372 (1997).
41. Fanales-Belasio, E. 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. 168, 197-206 (2002).
42. Bender, A., Sapp, M., Schuler, G., Steinman, R.M. & Bhardwaj, N. Improved methods for the generation of dendritic cells from nonproliferating progenitors in human blood. J. Immunol. Methods 196, 121-135 (1996).
43. Liu, Y.J. Dendritic cell subsets and lineages, and their functions in innate and adaptive immunity. Cell 106, 259-262 (2001).
44. + T cell frequencies by flow cytometry: evidence for a novel, antigen-specific homeostatic mechanism in HIV-associated immunodeficiency. J. Clin. Invest. 99, 1739-1750 (1997).
45. Poon, D.T., Wu, J. & Aldovini, A. Charged amino acid residues of human immunodeficiency virus type 1 nucleocapsid p7 protein involved in RNA packaging and infectivity. J. Virol. 70, 6607-6616 (1996).