HIV-induced T-cell syncytia release a two component T-helper cell chemoattractant composed of Nef and Tat

Journal of Cell Science

Volumn 112, Issue 22, 1999, Pages 3931-3941

  Shutt, Damon C ^a   Soll, David R ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

HIV; HIV induced syncytium; Nef; Tat; Two component chemoattractant

Indexed keywords

ANTIGEN P24; CD4 ANTIGEN; CHEMOATTRACTANT; GLYCOPROTEIN GP 120; LYMPHOCYTE ANTIGEN RECEPTOR; NEF PROTEIN; REV PROTEIN; TRANSACTIVATOR PROTEIN;

ARTICLE; CHEMOKINESIS; CHEMOTAXIS; DIFFUSION; HELPER CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; SYNCYTIUM; T LYMPHOCYTE; VIRUS CELL INTERACTION;

ANTIGENS, CD4; CELLS, CULTURED; CHEMOTACTIC FACTORS; CHEMOTAXIS; CULTURE MEDIA, CONDITIONED; DRUG SYNERGISM; GENE PRODUCTS, NEF; GENE PRODUCTS, TAT; GIANT CELLS; HIV-1; HUMANS; T-LYMPHOCYTES; T-LYMPHOCYTES, HELPER-INDUCER;

HUMAN IMMUNODEFICIENCY VIRUS; RNA VIRUSES;

EID: 0033490946     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (72)

1. Aiken, C., Konner, J., Landau, N. R., Lenburg, M. E. and Trono, D. (1994). Nef induces CD4 endocytosis: requirement for a critical dileucine motif in the membrane-proximal CD4 cytoplasmic domain. Cell 76, 853-864.
2. Albini, A., Errini, S., Benelli, R., Sforzini, S., Giunciuglio, D., Aluigi, M. G., Proudfoot, A. E., Alouani, S., Wells, T. N., Mariani, G., Rabin, R. L., Farber, J. M. and Noonan, D. M. (1998). HIV-1 Tat protein mimicry of chemokines. Proc. Nat. Acad. Sci. USA 95, 13151-13158.
3. Arthos, J., Deen, K. C., Chaikin, M. A., Fornwald, J. A., Sathe, G., Sattentau, Q. J., Clapham, P. R., Weiss, R. A., McDougal, J. S., Pietropaolo, C., Axel, R., Truneh, A., Maddon, P. J. and Sweet, R. W. (1989). Identification of the residues in human CD4 critical for the binding of HIV. Cell 57, 469-481.
4. Attanasio, R. J. S., Allan, J. S., Anderson, S. A., Chanh, T. C. and Kennedy, R. C. (1991). Anti-idiotypic antibody response to monoclonal anti-CD4 preparations in nonhuman primate species. J. Immunol. 146, 507-514.
5. Barr, P. J., Parkes, D., Sabin, E. A., Power, M. D., Gibson, H. L., Lee-Ng, C. T., Stephans, J. C., George-Nascimento, C., Sanchez-Pescador, R., Hallewell, R. A., Steimer, K. S. and Luciw, P. A. (1987). Expression of functional domains of the AIDS-associated retrovirus (ARV) in recombinant microorgansims. UCLA Symp. Mol. Cell. Biol. New Ser. 43, 205-219.
6. Benelli, R., Mortarini, R., Anichini, A., Giunciuglio, D., Noonan, D. M., Montalti, S., Tacchetti, C. and Albini, A. (1998). Monocyte-derived dendritic cells and monocytes migrate to HIV-Tat RGD and basic peptides. AIDS 12, 261-268.
7. Bleul, C. C., Farzan, M., Choe, H., Parolin, C., Clark-Lewis, I., Sodroski, J. and Springer, T. A. (1996). The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusin and blocks HIV-1 entry. Nature 382, 829-833.
8. Bohan, C. A, Kashanchi, F., Ensoli, B., Buonaguro, L., Boris-Lawrie, K. and Brady, J. N. (1992). Analysis of Tat transactivation of human immunodeficiency virus transcription in vitro. Gene Expr. 2, 391-407.
9. Boyden, S. V. (1962). The chemotactic effect of mixtures of antibody and antigen on polymorphonuclear leukocytes. J. Exp. Med. 115, 453-466.
10. Campbell, J. J., Qin, S., Bacon, K. B., Mackay, C. R. and Butcher, E. C. (1996). Biology of chemokine and classical chemoattractant receptors: differential requirements for adhesion-triggering versus chemotactic responses in lymphoid cells. J. Cell Biol. 134, 255-266.
11. Campioni, D., Corallini, A., Zauli, G., Possati, L., Altavilla, G. and Barbanti-Brodano, G. (1995). HIV type 1 extracellular Tat protein stimulates growth and protects cells of BK virus/tat transgenic mice from apoptosis. AIDS Res Hum Retroviruses 11, 1039-1048.
12. Cruikshank, W. W., Greenstein, J. L., Theodore, A. C. and Center, D. M. (1991). Lymphocyte chemoattractant factor induces CD4-dependent intracytoplasmic signaling in lymphocytes. J. Immunol. 146, 2928-2934.
13. Daniels, F. and Alberty, R. A. (1963). In Physical Chemistry, pp. 580-582. New York: John Wiley and Sons, Inc.
14. Dorfman, T., Bukovsky, A., Ohagen, A., Hoglund, S. and Gottlinger, H. G. (1994). Functional domains of the capsid protein of human immunodeficiency virus type 1. J. Virol. 68, 8180-8187.
15. Finkel, T. H., Tudor-Williams, G., Banda, N. K., Cotton, M. F., Curiel, T., Monks, C., Baba, T. W., Ruprecht, R. M. and Kupfer, A. (1995) Apoptosis occurs predominantly in bystander cells and not in productively infected cells of HIV- and SIV-infected lymph nodes. Nature Med. 1, 129-134.
16. Foxman, E. F., Campbell, J. J. and Butcher, E. C. (1997). Multistep navigation and the combinatorial control of leukocyte chemotaxis. J. Cell Biol. 139, 1349-1360.
17. Garcia, J. V. and Miller, A. D. (1991). Serine phosphorylation-independent downregulation of cell-surface CD4 by Nef. Nature 350, 508-511.
18. Gelderblom, H. R., Reupke, H. J. and Pauli, G. (1985). Loss of envelope antigens of HTLV-III/LAV, a factor in AIDS pathogenesis? Lancet 2, 1016-1017.
19. Graziani, A., Galimi, F., Medico, E., Cottone, E., Gramaglia, D., Boccoccio, C. and Comoglio, P. M. (1996). The HIV-I nef protein interferes with phosphatidylinositol 3-kinase activation. J. Biol. Chem. 271, 6590-6593.
20. Inoue, M., Koga, Y., Djordjijevic, D., Fukuma, T., Reddy, E. P., Yokayama, M. M and Sagawa, K. (1993). Down-regulation of CD-4 molecules by the expression of Nef: a quantitative analysis of CD4 antigens on the cell surface. Int. Immunol. 5, 1067-1073.
21. Janossy, G., Pinching, A. J., Bofill, M., Weber, J., McLaughlin, E., Ornstein, M., Ivory, K., Harris, J. R., Favrot, M. and Macdonald-Burns, D. C. (1985). An immunohistological approach to persistent lymphadenopathy and its relevance to AIDS. Clin. Exp. Immunol. 59, 257-266.
22. Kim, S. Y., Byrn, R., Groopman, J. and Baltimore, D. (1989). Temporal aspects of DNA and RNA synthesis during human immunodeficiency virus infection: evidence for differential gene expression. J. Virol. 63, 3708-3713.
23. Klotman, M. E., Kim, S., Buchbinder, A., DeRossi, A., Baltimore, D. and Wong-Staal, F. (1991). Kinetics of expression of multiply spliced RNA in early human immunodeficiency virus type 1 infection of lymphocytes and monocytes. Proc. Nat. Acad. Sci. USA 88, 5011-5015.
24. Kornfeld, H., W. W. Cruikshank, S. W. Pyle, J. S. Berman and Center, D. M. (1988). Lymphocyte activation by HIV-1 envelope glycoprotein. Nature 335, 445-448.
25. Kowolski, M. Potz, J., Basiropour, L., Dorfman, T., Goh, W. C., Terwiliger, E., Dayton, A., Rosen, C., Haseltine, W. and Sodroski, J. (1987). Functional regions of the envelope glycoprotein of human immunodeficiency virus type 1. Science 237, 1351-1355.
26. Lafrenie, R. M., Wahl, L. M., Epstein, J. S., Hewlett, I. K., Yamada, K. M. and Dhawan, S. (1996a). HIV-1 Tat modulates the function of monocytes and alters their interactions with microvessel endothelial cells. A mechanism of HIV pathogenesis. J. Immunol. 156, 1638-1645.
27. Lafrenie, R. M., Wahl, L. M., Epstein, J. S., Hewlett, I. K., Yamada, K. M. and Dhawan, S. (1996b). HIV-1 Tat protein promotes chemotaxis and invasive behavior by monocytes. J. Immunol. 157, 974-977.
28. Lauffenberger, D. A., Tranquillo, R. T. and Zigmond, S. H. (1988). Concentration gradients of chemotactic factors in chemotaxis assays. Meth. Enzymol. 162, pp. 84-101.
29. Lifson, J. D., Feinberg, M. B., Reyes, G. R., Rabin, L. Banapour, B., Chakrabarti, S., Moss, B., Wong-Staal, F., Steimer, K. and Engleman, E. G. (1986a). Induction of CD4-dependent cell fusion by the HTLV-III/LAV envelope glycoprotein. Nature 323, 725-728.
30. Lifson, J. D., Reyes, G. R., McGrath, M. S., Stein, B. S. and Engleman, E. G. (1986b). AIDS retrovirus induced cytopathology: Giant cell formation and involvement of CD4 antigen. Science 232, 1123-1127.
31. Loetscher, M., Gerber, B., Loetscher, P, Jones, S. A., Piali, L., Clark-Lewis, I., Baggiolini, M. and Moser, B. (1996). Chemokine receptor specific for IP-10 and mig: structure, function and expression in activated T-lymphocytes. J. Exp. Med. 184, 799-802.
32. Maron, M. J. (1982). Numerical Analysis: A Practical Approach. New York: Macmillan Press.
33. McDougal, J. S., Kennedy, M. S., Sligh, J. M., Cort, S. P., Mawle, A. and Nicholson, J. K. (1986). Binding of HTLV-III/LAV to T4+ cells by a complex of the 110K viral protein and the T4 molecule. Science 231, 382-385.
34. Mitola, S., Sozzani, S., Luini, W., Primo, L., Borsatti, A., Weich, H. and Bussolino, F. (1997). Tat-human immunodeficiency virus-1 induces human monocyte chemotaxis by activation of vascular endothelial growth factor receptor-1. Blood 90, 1365-1372.
35. Modesti, N., Garcia, J., DeBouck, C., Peterlin, M. and Gaynor, R. (1991). Transdominant tat mutants with altercations in the basic domain inhibit HIV-1 gene expression. New Biol. 3, 759-768.
36. + cells by HIV-induced T cell syncytia. AIDS Res. Hum. Retroviruses 11, 433-442.
37. O'Neill, G. J. and Parrott, D. M. V. (1977). Locomotion of human lymphoid cells. Effect of culture and ConA on T and non-T lymphocytes. Cell. Immunol. 33, 257-267.
38. Orsini, M. J., Debouck, C. M., Webb, C. L. and Lysko, P. G. (1996). Extracellular human immunodeficiency virus type 1 Tat protein promotes aggregation and adhesion of cerebellar neurons. J. Neurosci. 16, 2546-2552.
39. Pomerantz, R. J., Seshamma, T. and Trono, D. (1992). Efficient replication of human immunodeficiency virus type 1 requires a threshold level of Rev: potential implications for latency. J. Virol. 66, 1809-1813.
40. Rhodes, J. M. (1982). Measurement of chemotaxis in Boyden chamber filter assays. Is the checkerboard correction valid? J. Imunol. Meth. 49, 235-236.
41. Romero, I. A., Teixeira, A., Strosberg, A. D., Cazaubon, S. and Couraud, P. O. (1998). The HIV-1 Nef protein inhibits extracellular signal-regulated kinase-dependent DNA synthesis in a human astocytic cell line. J. Neurochem. 70, 778-785.
42. Rosenberg, Y. J., Zack, P. M., White, B. D., Papermaster, S. F., Elkins, W. R., Eddy, G. A. and Lewis, M. G. (1993). Decline in the CD4+ lymphocyte population in the blood of SIV-infected macaques is not reflected in lymph nodes. AIDS Res. Hum. Retroviruses 9, 639-646.
43. Sawai, E. T., Baur, A., Struble, H., Peterlin, B. M., Levy, J. A. and Cheng-Mayer, C. (1994). Human immunodeficiency virus type 1 Nef associates with a cellular serine kinase in T lymphocytes. Proc. Nat. Acad. Sci. USA 91, 1539-1543.
44. Schneider, J., Kaaden, O., Copeland, T. D., Orozslan, S. and Hunsmann, G. (1986). Shedding and interspecies type seroreactivity of the envelope glycoprotein gp120 of the human immunodeficiency virus. J. Gen. Virol. 67, 2533-2538.
45. Selby, M. J. and Peterlin, B. M. (1990). Trans-activation by HIV-1 Tat via a heterologous RNA binding protein. Cell 62, 769-776.
46. Shutt, D., Wessels, D., Wagenknecht, K., Chandrasekhar, A., Hitt, A., Luna, E. and Soll, D. R. (1995a). Ponticulin plays a role in the positional stabilization of pseudopods. J. Cell Biol. 131, 1495-1506.
47. Shutt, D. C., Stapleton, J. T., Kennedy, R. C. and Soll, D. R. (1995b). HIV-induced syncytia in peripheral blood cell cultures crawl by extending giant pseudopods. Cell. Immunol. 166, 261-274.
48. Shutt, D. C., Jenkins, L. M., Carolan, E. J., Stapleton, J., Daniels, K. J., Kennedy, R. C. and Soll, D. R. (1998). T cell syncytia induced by HIV release T cell chemoattractants: demonstration with a newly developed single cell chemotaxis chamber. J. Cell Sci. 111, 99-109.
49. Smith, S. D., Shatsky, M., Cohen, P. S., Warake, R., Link, M. P. and Glader, B. E. (1984). Monoclonal antibody and enzymatic profiles of human malignant T lymphoid cells and derived lines. Cancer Res. 44, 5657-5660.
50. Soll, D. R. and Kennedy, R. C. (1994). The role of T cell motilily and cytoskeletal reorganization in HIV-induced syncytium formation: a perspectus. AIDS Res. Hum. Retroviruses 10, 325-327.
51. Soll, D. R. (1995). The use of computers in understanding how cells crawl. Int. Rev. Cytol. 163, 43-104.
52. Soll, D. R. (1997). Researchers in cell motilily and the cyloskeleton can play major roles in understanding AIDS. Cell Motil. Cytoskel. 37, 91-97.
53. Soll, D. R. (1999). Computer-assisted three-dimensional reconstruction and motion analysis of living, crawling cells. Comput. Med. Imag. Graph. 23, 3-14.
54. Soll, D. R. and Voss, E. (1998). Two and three dimensional computer systems for analyzing how cells crawl. In Motion Analysis of Living Cells (ed. D. R. Soll and D. Wessels), pp. 25-52. New York: John Wiley, Inc.
55. Steimer, K. S., Puma, J. P., Powers, M. A., George-Nascimento, C., Stephans, J. C., Levy, J. A., Sanchez-Pescador, R., Luciw, P. A., Barr, P. J. and Hallewell, R. A. (1986). Differential antibody responses of individuals infected with AIDS-associated retroviruses surveyed using the viral core antigen p25 gag expressed in bacteria. Virology 150, 283-290.
56. Sylwester, A., Wessels, D., Anderson, S. A., Warren, R. Q., Shutt, D., Kennedy, R. and Soll, D. R. (1993). HIV-induced syncytia of a T cell line form single giant pseudopods and are motile. J. Cell Sci. 106, 941-953.
57. Sylwester, A., Shutt, D. C., Wessels, D., Stapleton, J. T., Stiles, J., Kennedy, R. C. and Soll, D. R. (1995). T cells and HIV-induced T cell syncytia exhibit the same motility cycle. J. Leuk. Biol. 57, 643-650.
58. Sylwester, A., Murphy, S., Shutt, D. and Soll, D. R. (1997). HIV-induced syncytia are self-perpetuating and the primary cause of T cell death in culture. J. Immunol. 158, 3996-4007.
59. Sylwester, A., Daniels, K. and Soll, D. R. (1998). The invasive and destructive behavior of HIV-induced T cell syncytia on collagen and endothelium. J. Leuk. Biol. 63, 233-244.
60. Tanford, C. (1961). Physical Chemistry of Molecules. Wiley Press, New York, New York.
61. Taub, D. D., Anver, M., Oppenheim, J. J., Longo, D. L. and Murphy, W. J. (1996). T lymphocyte recruitment by interleukin-8 (IL-8); IL-8 induced degranulation of neutrophils releases potent chemoattractants for human T lymphocytes both in vivo and in vitro. J. Clin. Invest. 97, 1931-1941.
62. Varnum, B., Edwards, K. and Soll, D. R. (1985). Dictyostelium amoebae alter motility differently in response to increasing versus decreasing temporal gradients of cAMP. J. Cell Biol. 101, 1-5.
63. Varnum-Finney, B., Edwards, K., Voss, E. and Soll, D. R. (1987). Amoebae of Dictyostelium discoideum respond to an increasing temporal gradient of the chemoattractant cAMP with a reduced frequency of turning: evidence for a temporal mechanism in amoeboid chemotaxis. Cell Motil. Cytoskel. 8, 7-17.
64. von Poblotzki, A., Wagner, R., Niedrig, M., Wanner, G., Wolf, H. and Modrow, S. (1993). Identification of a region in the Pr55gag-polyprotein essential for HIV-1 particle formation. Virology 193, 981-985.
65. Wang, L., Chen, J. J. Y., Gelman, B. B., Konig, R. and Cloyd, M. W. (1999). A novel mechanism of CD4 lymphocyte depletion involves effects of HIV on resting lymphocytes: induction of lymph node homing and apoptosis upon secondary signaling through homing receptors. J. Immunol. 162, 268-276.
66. Weissman, D., R. L. Rabin, J. Arthos, A. Ruppert, M. Dybul, R. Swofford, S. Venkatesan, J. M. Farber and Fauci, A. S. (1997). Macrophage-trophic HIV and SIV envelope proteins induce a signal through the CCR5 chemokine receptor. Nature 389, 981-985.
67. Wessels, D., Murray, J. and Soll, D. R. (1992). The complex behavior cycle of chemotaxing Dictyostelium amoebae is regulated primarily by the temporal dynamics of the natural wave. Cell Motil. Cytoskel. 23, 145-156.
68. Wilkinson, P. C. (1988). Micropore filter methods for measuring leukocyte chemotaxis. Meth. Enzymol. 162, 38-50.
69. Zigmond, S. H. and Hirsch, J. G. (1973). Leukocyte locomotion and chemotaxis. New method for evaluation, and demonstration of a cell-derived chemotactic factor. J. Exp. Med. 137, 387-410.
70. Zigmond, S. H. (1977). The ability of polymorphonuclear leukocytes to orient in gradients of chemotactic factors. J. Cell Biol. 75, 606-616.
71. Zigmond, S. H. (1978). A new visual assay of leukocyte chemotaxis. In Leukocyte Chemotaxis: Methods, Physiology and Clinical Implication (ed. J. I. Gallin and P. G. Quie), pp. 57-66. New York: Raven Press.
72. Zigmond, S. H. and Sullivan, S. J. (1979). Sensory adaptation of leukocytes to chemotactic peptides. J. Cell. Biol. 82, 517-527.