NK cell lysis of HIV-1-infected autologous CD4 primary T cells: Requirement for IFN-mediated NK activation by plasmacytoid dendritic cells

Journal of Immunology

Volumn 179, Issue 4, 2007, Pages 2097-2104

  Tomescu, Costin ^a   Chehimi, Jihed ^a   Maino, Vernon C ^b   Montaner, Luis J ^a  

^a WISTAR INSTITUTE   (United States)

^b BD BIOSCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CPG OLIGODEOXYNUCLEOTIDE; INTERFERON; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NEUTRALIZING ANTIBODY; HLA ANTIGEN CLASS 1; OLIGODEOXYRIBONUCLEOTIDE; TLR9 PROTEIN, HUMAN; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG;

ARTICLE; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOLYSIS; DENDRITIC CELL; DOWN REGULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; EXOCYTOSIS; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; CELL CULTURE; CLINICAL TRIAL; COCULTURE; DRUG EFFECT; DRUG POTENTIATION; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; INNATE IMMUNITY; LYMPHOCYTE ACTIVATION; PLASMA CELL; VIROLOGY;

CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; COCULTURE TECHNIQUES; DENDRITIC CELLS; DOWN-REGULATION; HISTOCOMPATIBILITY ANTIGENS CLASS I; HIV INFECTIONS; HIV-1; HUMANS; IMMUNITY, NATURAL; INTERFERONS; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; OLIGODEOXYRIBONUCLEOTIDES; PLASMA CELLS; TOLL-LIKE RECEPTOR 9;

EID: 34848845812     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.4.2097     Document Type: Article

References (48)

1. Vollmer, J., R. Weeratna, P. Payette, M. Jurk, C. Schetter, M. Laucht, T. Wader, S. Tluk, M. Liu, H. L. Davis, and A. M. Krieg. 2004. Characterization of three CpG oligodeoxynucleotide classes with distinct immunostimulatory activities. Eur. J. Immunol. 34: 251-262.
2. Kerkmann, M., S. Rothenfusser, V. Hornung, A. Towarowski, M. Wagner, A. Sarris, T. Giese, S. Endres, and G. Hartmann. 2003. Activation with CpG-A and CpG-B oligonucleotides reveals two distinct regulatory pathways of type I IFN synthesis in human plasmacytoid dendritic cells. J. Immunol. 170: 4465-4474.
3. Fitzgerald-Bocarsly, P. 2002. Natural interferon-α producing cells: the plasmacytoid dendritic cells. BioTechniques (Suppl.) 33: 16-29.
4. Krug, A., S. Rothenfusser, V. Hornung, B. Jahrsdorfer, S. Blackwell, Z. K. Ballas, S. Endres, A. M. Krieg, and G. Hartmann. 2001. Identification of CpG oligonucleotide sequences with high induction of IFN-α/β in plasmacytoid dendritic cells. Eur. J. Immunol. 31: 2154-2163.
5. Smit, J. J., B. D. Rudd, and N. W. Lukacs. 2006. Plasmacytoid dendritic cells inhibit pulmonary immunopathology and promote clearance of respiratory syncytial virus. J. Exp. Med. 203: 1153-1159.
6. Yoneyama, H., K. Matsuno, E. Toda, T. Nishiwaki, N. Matsuo, A. Nakano, S. Narumi, B. Lu, C. Gerard, S. Ishikawa, and K. Matsushima. 2005. Plasmacytoid DCs help lymph node DCs to induce anti-HSV CTLs. J. Exp. Med. 202: 425-435.
7. Almeida, M., M. Cordero, J. Almeida, and A. Orfao. 2005. Different subsets of peripheral blood dendritic cells show distinct phenotypic and functional abnormalities in HIV-1 infection. AIDS 19: 261-271.
8. Chehimi, J., D. E. Campbell, L. Azzoni, D. Bacheller, E. Papasavvas, G. Jerandi, K. Mounzer, J. Kostman, G. Trinchieri, and L. J. Montaner. 2002. Persistent decreases in blood plasmacytoid dendritic cell number and function despite effective highly active antiretroviral therapy and increased blood myeloid dendritic cells in HIV-infected individuals. J. Immunol. 168: 4796-4801.
9. Feldman, S., D. Stein, S. Amrute, T. Denny, Z. Garcia, P. Kloser, Y. Sun, N. Megjugorac, and P. Fitzgerald-Bocarsly. 2001. Decreased interferon-α production in HIV-infected patients correlates with numerical and functional deficiencies in circulating type 2 dendritic cell precursors. Clin. Immunol. 101: 201-210.
10. - plasmacytoid dendritic cells in patients with HIV-1 infection correlates with HIV-1 RNA virus load. Blood 98: 2574-2576.
11. Soumelis, V., I. Scott, F. Gheyas, D. Bouhour, G. Cozon, L. Cotte, L. Huang, J. A. Levy, and Y. J. Liu. 2001. Depletion of circulating natural type 1 interferon-producing cells in HIV-infected AIDS patients. Blood 98: 906-912.
12. Pacanowski, J., L. Develioglu, I. Kamga, M. Sinet, M. Desvarieux, P. M. Girard, and A. Hosmalin. 2004. Early plasmacytoid dendritic cell changes predict plasma HIV load rebound during primary infection. J. Infect. Dis. 190: 1889-1892.
13. - cells with low lytic activity. J. Acquired Immune Defic. Syndr. Hum. Retrovirol. 10: 331-340.
14. + natural killer cell subset during HIV infection. Cytometry 22: 10-15.
15. Sirianni, M. C., I. Mezzaroma, F. Aiuti, and A. Moretta. 1994. Analysis of the cytolytic activity mediated by natural killer cells from acquired immunodeficiency syndrome patients in response to phytohemagglutinin or anti-CD16 monoclonal antibody. Eur. J. Immunol. 24: 1874-1878.
16. Azzoni, L., E. Papasavvas, J. Chehimi, J. R. Kostman, K. Mounzer, J. Ondercin, B. Perussia, and L. J. Montaner. 2002. Sustained impairment of IFN-γ secretion in suppressed HIV-infected patients despite mature NK cell recovery: evidence for a defective reconstitution of innate immunity. J. Immunol. 168: 5764-5770.
17. Ullum, H., P. C. Gotzsche, J. Victor, E. Dickmeiss, P. Skinhoj, and B. K. Pedersen. 1995. Defective natural immunity: an early manifestation of human immunodeficiency virus infection. J. Exp. Med. 182: 789-799.
18. Mavilio, D., J. Benjamin, M. Daucher, G. Lombardo, S. Kottilil, M. A. Planta, E. Marcenaro, C. Bottino, L. Moretta, A. Moretta, and A. S. Fauci. 2003. Natural killer cells in HIV-1 infection: dichotomous effects of viremia on inhibitory and activating receptors and their functional correlates. Proc. Natl. Acad. Sci. USA 100: 15011-15016.
19. De Maria, A., M. Fogli, P. Costa, G. Murdaca, F. Puppo, D. Mavilio, A. Moretta, and L. Moretta. 2003. The impaired NK cell cytolytic function in viremic HIV-1 infection is associated with a reduced surface expression of natural cytotoxicity receptors (NKp46, NKp30 and NKp44). Eur. J. Immunol. 33: 2410-2418.
20. Huang, X. L., Z. Fan, T. Murayama, and C. Rinaldo. 1995. Enhancement of natural killer cell activity in human immunodeficiency virus-infected subjects by in vitro treatment with biologic response modifier OK-432. Clin. Diagn. Lab. Immunol. 2: 91-97.
21. Portales, P., J. Reynes, V. Pinet, R. Rouzier-Panis, V. Baillat, J. Clot, and P. Corbeau. 2003. Interferon-α restores HIV-induced alteration of natural killer cell perforin expression in vivo. AIDS 17: 495-504.
22. Chehimi, J., and G. Trinchieri. 1994. Interleukin-12: a bridge between innate resistance and adaptive immunity with a role in infection and acquired immunodeficiency. J. Clin. Immunol. 14: 149-161.
23. Feldman, M., D. Howell, and P. Fitzgerald-Bocarsly. 1992. Interferon-α-dependent and -independent participation of accessory cells in natural killer cell-mediated lysis of HSV-1-infected fibroblasts. J. Leukocyte Biol. 52: 473-482.
24. +) cells require the presence of accessory cells or factors for the lysis of herpes simplex virus-infected fibroblasts but not herpes simplex virus-infected Raji. J. Immunol. 143: 1318-1326.
25. + accessory cells in natural killing of cytomegalovirus-infected fibroblasts. J. Exp. Med. 164: 180-195.
26. + cells in natural killing of herpesvirus-infected fibroblasts. J. Immunol. 139: 2799-2802.
27. Perussia, B., V. Fanning, and G. Trinchieri. 1985. A leukocyte subset bearing HLA-DR antigens is responsible for in vitro interferon production in response to viruses. Nat. Immun. Cell Growth Regul. 4: 120-137.
28. Schmidt, B., B. M. Ashlock, H. Foster, S. H. Fujimura, and J. A. Levy. 2005. HIV-infected cells are major inducers of plasmacytoid dendritic cell interferon production, maturation, and migration. Virology 343: 256-266.
29. Yonezawa, A., R. Morita, A. Takaori-Kondo, N. Kadowaki, T. Kitawaki, T. Hori, and T. Uchiyama. 2003. Natural α interferon-producing cells respond to human immunodeficiency virus type 1 with α interferon production and maturation into dendritic cells. J. Virol. 77: 3777-3784.
30. Jaattela, M. 1990. Effects of heat shock on cytolysis mediated by NK cells, LAK cells, activated monocytes and TNFs α and β. Scand. J. Immunol. 31: 175-182.
31. Warren, H. S., A. L. Jones, C. Freeman, J. Bettadapura, and C. R. Parish. 2005. Evidence that the cellular ligand for the human NK cell activation receptor NKp30 is not a heparan sulfate glycosaminoglycan. J. Immunol. 175: 207-212.
32. Bonaparte, M. I., and E. Barker. 2004. Killing of human immunodeficiency virus-infected primary T-cell blasts by autologous natural killer cells is dependent on the ability of the virus to alter the expression of major histocompatibility complex class I molecules. Blood 104: 2087-2094.
33. Bonaparte, M. I., and E. Barker. 2003. Inability of natural killer cells to destroy autologous HIV-infected T lymphocytes. AIDS 17: 487-494.
34. Cohen, G. B., R. T. Gandhi, D. M. Davis, O. Mandelboim, B. K. Chen, J. L. Strominger, and D. Baltimore. 1999. The selective down-regulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells. Immunity 10: 661-671.
35. Nattermann, J., H. D. Nischalke, V. Hofmeister, B. Kupfer, G. Ahlenstiel, G. Feldmann, J. Rockstroh, E. H. Weiss, T. Sauerbruch, and U. Spengler. 2005. HIV-1 infection leads to increased HLA-E expression resulting in impaired function of natural killer cells. Antivir. Ther. 10: 95-107.
36. Martini, F., C. Agrati, G. D'Offizi, and F. Poccia. 2005. HLA-E up-regulation induced by HIV infection may directly contribute to CD94-mediated impairment of NK cells. Int. J. Immunopathol. Pharmacol. 18: 269-276.
37. Alter, G., J. M. Malenfant, and M. Altfeld. 2004. CD107a as a functional marker for the identification of natural killer cell activity. J. Immunol. Methods 294: 15-22.
38. Huard, B., L. Karlsson, and F. Triebel. 2001. KIR down-regulation on NK cells is associated with down-regulation of activating receptors and NK cell inactivation. Eur. J. Immunol. 31: 1728-1735.
39. Groh, V., J. Wu, C. Yee, and T. Spies. 2002. Tumor-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 419: 734-738.
40. Song, H., J. Kim, D. Cosman, and I. Choi. 2006. Soluble ULBP suppresses natural killer cell activity via down-regulating NKG2D expression. Cell. Immunol. 239: 22-30.
41. Kataoka, T., N. Shinohara, H. Takayama, K. Takaku, S. Kondo, S. Yonehara, and K. Nagai. 1996. Concanamycin A, a powerful tool for characterization and estimation of contribution of perforin- and Fas-based lytic pathways in cell-mediated cytotoxicity. J. Immunol. 156: 3678-3686.
42. Groot, F., T. M. van Capel, M. L. Kapsenberg, B. Berkhout, and E. C. de Jong. 2006. Opposing roles of blood myeloid and plasmacytoid dendritic cells in HIV-1 infection of T cells: transmission facilitation versus replication inhibition. Blood 108: 1957-1964.
43. + T cells during HIV-1 infection: a gp41 peptide induces the expression of an NKp44 ligand. Proc. Natl. Acad. Sci. USA 102: 10981-10986.
44. Vieillard, V., D. Costagliola, A. Simon, and P. Debre. 2006. Specific adaptive humoral response against a gp41 motif inhibits CD4 T-cell sensitivity to NK lysis during HIV-1 infection. AIDS 20: 1795-1804.
45. Kamga, I., S. Kahi, L. Develioglu, M. Lichtner, C. Maranon, C. Deveau, L. Meyer, C. Goujard, P. Lebon, M. Sinet, and A. Hosmalin. 2005. Type I interferon production is profoundly and transiently impaired in primary HIV-1 infection. J. Infect. Dis. 192: 303-310.
46. Scott-Algara, D., L. X. Truong, P. Versmisse, A. David, T. T. Luong, N. V. Nguyen, I. Theodorou, F. Barre-Sinoussi, and G. Pancino. 2003. Cutting edge: increased NK cell activity in HIV-1-exposed but uninfected Vietnamese intravascular drug users. J. Immunol. 171: 5663-5667.
47. Hatzakis, A., P. Gargalianos, V. Kiosses, M. Lazanas, V. Sypsa, C. Anastassopoulou, V. Vigklis, H. Sambatakou, C. Botsi, D. Paraskevis, and C. Stalgis. 2001. Low-dose IFN-α monotherapy in treatment-naive individuals with HIV-1 infection: evidence of potent suppression of viral replication. J. Interferon Cytokine Res. 21: 861-869.
48. Martin, M. P., X. Gao, J. H. Lee, G. W. Nelson, R. Detels, J. J. Goedert, S. Buchbinder, K. Hoots, D. Vlahov, J. Trowsdale, et al. 2002. Epistatic interaction between KIR3DS1 and HLA-B delays the progression to AIDS. Nat. Genet. 31: 429-434.