IL-21 enhances NK cell functions and survival in healthy and HIV-infected patients with minimal stimulation of viral replication

Journal of Leukocyte Biology

Volumn 87, Issue 5, 2010, Pages 857-867

  Iannello, Alexandre ^a,d   Boulassel, Mohamed Rachid ^b   Samarani, Suzanne ^a,d   Tremblay, Cécile ^c,d   Toma, Emil ^c,d   Routy, Jean Pierre ^b   Ahmad, Ali ^a,d  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^c CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^d UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

LFA 1; MAPK; Perforin; STAT 3

Indexed keywords

CD16 ANTIGEN; CD56 ANTIGEN; CYTOKINE RECEPTOR; INTERLEUKIN 21; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MITOGEN ACTIVATED PROTEIN KINASE; PERFORIN; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN KINASE B; STAT3 PROTEIN; INTERLEUKIN 21 RECEPTOR; INTERLEUKIN DERIVATIVE;

ARTICLE; CELL FUNCTION; CELL PROLIFERATION; CELL VIABILITY; COCULTURE; CYTOTOXICITY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SURVIVAL; VIRUS REPLICATION; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; BIOSYNTHESIS; CD4+ T LYMPHOCYTE; CELL CULTURE; CELL SEPARATION; DRUG EFFECT; FLOW CYTOMETRY; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ANTIBODY-DEPENDENT CELL CYTOTOXICITY; BLOTTING, WESTERN; CD4-POSITIVE T-LYMPHOCYTES; CELL SEPARATION; CELLS, CULTURED; COCULTURE TECHNIQUES; FLOW CYTOMETRY; HIV INFECTIONS; HIV-1; HUMANS; INTERLEUKINS; KILLER CELLS, NATURAL; RECEPTORS, INTERLEUKIN-21; SIGNAL TRANSDUCTION; VIRUS REPLICATION;

EID: 77952540913     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.1009701     Document Type: Article

References (40)

1. Spolski, R., Leonard, W. J. (2008) Interleukin-21: basic biology and implications for cancer and autoimmunity. Annu. Rev. Immunol. 26, 57-79.
2. Parrish-Novak, J., Dillon, S. R., Nelson, A., Hammond, A., Sprecher, C., Gross, J. A., Johnston, J., Madden, K., Xu, W., West, J., et al. (2000) Interleukin 21 and its receptor are involved in NK cell expansion and regulation of lymphocyte function. Nature 408, 57-63.
3. Onoda, T., Rahman, M., Nara, H., Araki, A., Makabe, K., Tsumoto, K., Kumagai, I., Kudo, T., Ishii, N., Tanaka, N., Sugamura, K., Hayasaka, K., Asao, H. (2007) Human CD4+ central and effector memory T cells produce IL-21: effect on cytokine-driven proliferation of CD4+ T cell subsets. Int. Immunol. 19, 1191-1199.
4. Yi, J. S., Du, M., Zajac, A. J. (2009) A vital role for interleukin-21 in the control of a chronic viral infection. Science 324, 1572-1576.
5. Nutt, S. L., Brady, J., Hayakawa, Y., Smyth, M. (2004) Interleukin 21: a key player in lymphocyte maturation. Crit. Rev. Immunol. 24, 239-250.
6. Burgess, S. J., Marusina, A. I., Pathmanathan, I., Borrego, F., Coligan, J. E. (2006) IL-21 down-regulates NKG2D/DAP10 expression on human NK and CD8+ T cells. J. Immunol. 176, 1490-1497.
7. Eriksen, K. W., Søndergaard, H., Woetmann, A., Krejsgaard, T., Skak, K., Geisler, C., Wasik, M., Odum, N. (2009) The combination of IL-21 and IFN-α boosts STAT3 activation, cytotoxicity and experimental tumor therapy. Mol. Immunol. 46, 812-820.
8. Skak, K., Frederiksen, K., Lundsgaard, D. (2008) Interleukin-21 activates human natural killer cells and modulates their surface receptor expression. Immunology 123, 575-583. (Pubitemid 351280971)
9. Strengell, M., Matikainen, S., Siren, J., Lehtonen, A., Foster, D., Julkunen, I., Sareneva, T. (2003) IL-21 in synergy with IL-15 or IL-18 enhances IFN-{γ} production in human NK and T cells. J. Immunol. 170, 5464-5469. (Pubitemid 36617833)
10. Wang, G., Tschoi, M., Spolski, R., Lou, Y., Ozaki, K., Feng, C., Kim, G., Leonard, W. J., Hwu, P. (2003) In vivo antitumor activity of interleukin 21 mediated by natural killer cells. Cancer Res. 63, 9016-9022.
11. Iannello, A., Debbeche, O., Samarani, S., Ahmad, A. (2008) Antiviral NK cell responses in HIV infection: II. viral strategies for evasion and lessons for immunotherapy and vaccination. J. Leukoc. Biol. 84, 27-49.
12. Scott-Algara, D., Truong, L. X., Versmisse, P., David, A., Luong, T. T., Nguyen, N. V., Theodorou, I., Barre-Sinoussi, F., Pancino, G. (2003) Cutting edge: increased NK cell activity in HIV-1-exposed but uninfected Vietnamese intravascular drug users. J. Immunol. 171, 5663-5667.
13. Mavilio, D., Lombardo, G., Benjamin, J., Kim, D., Follman, D., Marcenaro, E., O'Shea, M. A., Kinter, A., Kovacs, C., Moretta, A., Fauci, A. S. (2005) Characterization of CD56-/CD16+ natural killer (NK) cells: a highly dysfunctional NK subset expanded in HIV-infected viremic individuals. Proc. Natl. Acad. Sci. USA 102, 2886-2891.
14. Iannello, A., Tremblay, C., Routy, J., Boulassel, M., Toma, E., Ahmad, A. (2008) Decreased levels of circulating IL-21 in HIV-infected AIDS patients: correlation with CD4+ T cell counts. Viral Immunol. 21, 385-388.
15. Iannello, A., Boulassel, M., Samarani, S., Debbeche, O., Tremblay, C., Toma, E., Routy, J., Ahmad, A. (2010) Dynamics and consequences of IL-21 production in HIV-infected individuals: a longitudinal and cross-sectional study. J. Immunol. 184, 114-126.
16. Strbo, N., de Armas, L., Liu, H., Kolber, M., Lichtenheld, M., Pahwa, S. (2008) IL-21 augments natural killer effector functions in chronically HIV-infected individuals. AIDS 22, 1551-1560.
17. Ahmad, A., Morisset, R., Thomas, R., Menezes, J. (1994) Evidence for a defect of antibody-dependent cellular cytotoxic (ADCC) effector function and anti-HIV gp120/41-specific ADCC-mediating antibody titres in HIV-infected individuals. J. Acquir. Immune Defic. Syndr. 7, 428-437.
18. Zhang, Y., Stastny, P. (2006) MICA antigens stimulate T cell proliferation and cell-mediated cytotoxicity. Hum. Immunol. 67, 215-222.
19. Wendt, K., Wilk, E., Buyny, S., Schmidt, R.E., Jacobs, R. (2007) Interleukin-21 differentially affects human natural killer cell subsets. Immunology 122, 486-495.
20. Brady, J., Hayakawa, Y., Smyth, M., Nutt, S. (2004) IL-21 induces the functional maturation of murine NK cells. J. Immunol. 172, 2048-2058. (Pubitemid 38182350)
21. Roda, J. M., Parihar, R., Lehman, A., Mani, A., Tridandapani, S., Carson III, W. E. (2006) Interleukin-21 enhances NK cell activation in response to antibody-coated targets. J. Immunol. 177, 120-129.
22. Iannello, A., Ahmad, A. (2005) Role of antibody-dependent cell-mediated cytotoxicity in the efficacy of therapeutic anti-cancer monoclonal antibodies. Cancer Metastasis Rev. 24, 487-499. (Pubitemid 43096997)
23. Strengell, M., Sareneva, T., Foster, D., Julkunen, I., Matikainen, S. (2002) IL-21 up-regulates the expression of genes associated with innate immunity and Th1 response. J. Immunol. 169, 3600-3605.
24. Grund, E. M., Spyropoulos, D., Watson, D., Muise-Helmericks, R. (2005) Interleukins 2 and 15 regulate Ets1 expression via ERK1/2 and MNK1 in human natural killer cells. J. Biol. Chem. 280, 4772-4778.
25. Naora, H., Gougeon, M. (1999) Interleukin-15 is a potent survival factor in the prevention of spontaneous but not CD95-induced apoptosis in CD4 and CD8 T lymphocytes of HIV-infected individuals. Correlation with its ability to increase BCL-2 expression. Cell Death Differ. 6, 1002-1011.
26. Naora, H., Gougeon, M. (1999) Enhanced survival and potent expansion of the natural killer cell population of HIV-infected individuals by exogenous interleukin-15. Immunol. Lett. 68, 359-367.
27. Vassena, L., Proschan, M., Fauci, A., Lusso, P. (2007) Interleukin 7 reduces the levels of spontaneous apoptosis in CD4+ and CD8+ T cells from HIV-1-infected individuals. Proc. Natl. Acad. Sci. USA 104, 2355-2360.
28. Pahwa, S. (2007) Role of common γ chain utilizing cytokines for immune reconstitution in HIV infection. Immunol. Res. 38, 373-386.
29. Ostiguy, V., Allard, E.-L., Marquis, M., Leignadier, J., Labrecque, N. (2007) IL-21 promotes T lymphocyte survival by activating the phosphatidylinositol-3 kinase signaling cascade. J. Leukoc. Biol. 82, 645-656.
30. White, L., Krishnan, S., Strbo, N., Liu, H., Kolber, M. A., Lichtenheld, M. G., Pahwa, R. N., Pahwa, S. (2007) Differential effects of IL-21 and IL-15 on perforin expression, lysosomal degranulation, and proliferation in CD8 T cells of patients with human immunodeficiency virus-1 (HIV). Blood 109, 3873-3880. (Pubitemid 46641739)
31. Bayard-McNeeley, M., Doo, H., He, S., Hafner, A., Johnson Jr., W. D., Ho, J. L. (1996) Differential effects of interleukin-12, interleukin-15, and interleukin- 2 on human immunodeficiency virus type 1 replication in vitro. Clin. Diagn. Lab. Immunol. 3, 547-553.
32. Patki, A. H., Quiñones-Mateu, M., Dorazio, D., Yen-Lieberman, B., Boom, W., Thomas, E., Lederman, M. (1996) Activation of antigen-induced lymphocyte proliferation by interleukin-15 without the mitogenic effect of interleukin-2 that may induce human immunodeficiency virus-1 expression. J. Clin. Invest. 98, 616-621.
33. Smithgall, M. D., Wong, J. G., Critchett, K. E., Haffar, O. K. (1996) IL-7 up-regulates HIV-1 replication in naturally infected peripheral blood mononuclear cells. J. Immunol. 156, 2324-2330. (Pubitemid 26087464)
34. Bonaparte, M. I., Barker, E. (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.
35. Fogli, M., Mavilio, D., Brunetta, E., Varchetta, S., Ata, K., Roby, G., Kovacs, C., Follmann, D., Pende, D., Ward, J., Barker, E., Marcenaro, E., Moretta, A., Fauci, A. (2008) Lysis of endogenously infected CD4+ T cell blasts by rIL-2 activated autologous natural killer cells from HIV-infected viremic individuals. PLoS Pathog. 4, e1000101.
36. Barber, D. F., Faure, M., Long, E. O. (2004) LFA-1 contributes an early signal for NK cell cytotoxicity. J. Immunol. 173, 3653-3659. (Pubitemid 39280725)
37. Liu, D., Bryceson, Y. T., Meckel, T., Vasiliver-Shamis, G., Dustin, M. L., Long, E. O. (2009) Integrin-dependent organization and bidirectional vesicular traffic at cytotoxic immune synapses. Immunity 31, 99-109.
38. Perez, O. D., Mitchell, D., Jager, G. C., Nolan, G. P. (2004) LFA-1 signaling through p44/42 is coupled to perforin degranulation in CD56+CD8+ natural killer cells. Blood 104, 1083-1093. (Pubitemid 39038029)
39. Hioe, C. E., Chien Jr., P. C., Lu, C., Springer, T. A., Wang, X-H., Bandres, J., Tuen, M. (2001) LFA-1 expression on target cells promotes human immunodeficiency virus type 1 infection and transmission. J. Virol. 75, 1077-1082. (Pubitemid 32037313)
40. Davis, I. D., Brady, B., Kefford, R., Millward, M., Cebon, J., Skrumsager, B., Mouritzen, U., Hansen, L., Skak, K., Lundsgaard, D., Frederiksen, K., Kristjansen, P., McArthur, G. (2009) Clinical and biological efficacy of recombinant human interleukin-21 in patients with stage IV malignant melanoma without prior treatment: a phase IIa trial. Clin. Cancer Res. 15, 2123-2129.