1887

Abstract

Chimpanzees are susceptible to human immunodeficiency virus type-1 (HIV-1) and develop persistent infection but generally do not progress to full-blown AIDS. Several host and immunological factors have been implicated in mediating resistance to disease progression. Chimpanzees have a higher prevalence of circulating natural killer (NK) cells than humans; however, their role in mediating resistance to disease progression is not well understood. Furthermore, NK cell survival and activity have been shown to be dependent on interleukin-15 (IL-15). Accordingly, the influence of IL-15 on NK cell activity and gamma interferon (IFN-) production was evaluated in naive and HIV-1-infected chimpanzees. stimulation of whole-blood cultures with recombinant gp120 (rgp120) resulted in enhanced IFN- production predominantly by the CD3 CD8 subset of NK cells, and addition of anti-IL-15 to the system decreased IFN- production. Moreover, stimulation with recombinant IL-15 (rIL-15) augmented IFN- production from this subset of NK cells and increased NK cell cytotoxic activity. Stimulation with rgp120 also resulted in a 2- to 7-fold increase in IL-15 production. These findings suggest that chimpanzee CD3 CD8 NK cells play a vital role in controlling HIV-1 infection by producing high levels of IFN-, and that IL-15 elicits IFN- production in this subpopulation of NK cells in HIV-1-infected chimpanzees.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.82154-0
2007-02-01
2019-12-08
Loading full text...

Full text loading...

/deliver/fulltext/jgv/88/2/641.html?itemId=/content/journal/jgv/10.1099/vir.0.82154-0&mimeType=html&fmt=ahah

References

  1. Addo, M. M., Yu, X. G., Rathod, A., Cohen, D., Eldridge, R. L., Strick, D., Johnston, M. N., Corcoran, C., Wurcel, A. G. & other authors ( 2003; ). Comprehensive epitope analysis of human immunodeficiency virus type 1 (HIV-1)-specific T-cell responses directed against the entire expressed HIV-1 genome demonstrate broadly directed responses, but no correlation to viral load. J Virol 77, 2081–2092.[CrossRef]
    [Google Scholar]
  2. Ahmad, R., Sindhu, S. T., Toma, E., Morisset, R. & Ahamad, A. ( 2003; ). Studies on the production of IL-15 in HIV infected/AIDS patients. J Clin Immunol 23, 81–90.[CrossRef]
    [Google Scholar]
  3. Alter, G., Malenfant, J. M., Delabre, R. M., Burgett, N. C., Yu, X. G., Lichterfeld, M., Zaunders, J. & Altfeld, M. ( 2004; ). Increased natural killer cell activity in viremic HIV-1 infection. J Immunol 173, 5305–5311.[CrossRef]
    [Google Scholar]
  4. Azzoni, L., Papasavvas, E., Chehimi, J., Kostman, J. R., Mounzer, K., Ondercin, J., Perussia, B. & Montaner, L. J. ( 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.[CrossRef]
    [Google Scholar]
  5. Balla-Jhagjhoorsingh, S. S., Koopman, G., Mooij, P., Haaksama, T. G. M., Teeuwsen, V. J. P., Bontrop, R. E. & Heeney, J. L. ( 1999; ). Conserved CTL epitopes shared between HIV-infected human long-term survivors and chimpanzees. J Immunol 162, 2308–2314.
    [Google Scholar]
  6. Bamford, R. N., Battiata, A. P., Burton, J. D., Sharma, H. & Waldmann, T. A. ( 1996; ). Interleukin (IL) 15/IL-T production by the adult T-cell lymphotrophic virus type I R region/IL-15 fusion message that lacks many upstream AUGs that normally attenuate IL-15 mRNA translation. Proc Natl Acad Sci U S A 93, 2897–2902.[CrossRef]
    [Google Scholar]
  7. Betts, M. R., Ambrozak, D. R., Douek, D. C., Bonhoeffer, S., Brenchley, J. M., Casazza, J. P., Koup, R. A. & Picker, L. J. ( 2001; ). Analysis of total human immunodeficiency virus (HIV)-specific CD4+ and CD8+ T-cell responses: relationship to viral load in untreated HIV infection. J Virol 75, 11983–11991.[CrossRef]
    [Google Scholar]
  8. Castelli, J., Thomas, E. K., Gilliet, M., Liu, Y. & Levy, J. A. ( 2004; ). Mature dendritic cells can enhance CD8+ cell noncytotoxic anti-HIV responses: the role of IL-15. Blood 103, 2699–2704.[CrossRef]
    [Google Scholar]
  9. Castro, B. A., Homsy, J., Lennette, E., Murthy, K. K., Eichberg, J. W. & Levy, J. A. ( 1992; ). HIV-1 expression in chimpanzees can be activated by CD8+ cell depletion of CMV infection. Clin Immunol Immunopathol 65, 227–233.[CrossRef]
    [Google Scholar]
  10. Davis, I. C., Girard, M. & Fultz, P. N. ( 1998; ). Loss of CD4+ T cells in human immunodeficiency virus type-1 infected chimpanzees is associated with increased lymphocyte apoptosis. J Virol 72, 4623–4632.
    [Google Scholar]
  11. Di Rienzo, A. M., Furlini, G., Olivier, R., Ferris, S., Heeney, J. & Montagnier, L. ( 1994; ). Different proliferative response of human and chimpanzee lymphocyte after contact with human immunodeficiency virus type 1 gp120. Eur J Immunol 24, 34–40.[CrossRef]
    [Google Scholar]
  12. Droge, W., Murthy, K. K., Stahl-Hennig, C., Hartung, S., Plesker, R., Rouse, S., Peterhans, E., Kinscherf, R., Fischbach, T. & Eck, H. P. ( 1993; ). Plasma amino acid dysregulation after lentiviral infection. AIDS Res Hum Retroviruses 9, 807–809.[CrossRef]
    [Google Scholar]
  13. Dunne, J., Lynch, S., O'Farrelly, C., Todryk, S., Hegarty, F. E., Feighery, C. & Doherty, D. G. ( 2001; ). Selective expansion and partial activation of human NK cells and NK receptor-positive T cells by IL-2 and IL-15. J Immunol 167, 3129–3138.[CrossRef]
    [Google Scholar]
  14. Edwards, B. H., Bansal, A., Sabbaj, S., Bakari, J., Mulligan, M. J. & Goepfert, P. A. ( 2002; ). Magnitude of functional CD8+ T-cell responses to the gag protein of human immunodeficiency virus type 1 correlates inversely with viral load in plasma. J Virol 76, 2298–2305.[CrossRef]
    [Google Scholar]
  15. Fehniger, T. A., Shah, M. H., Turner, M. J., VanDeusen, J. B., Whitman, S. P., Copper, M. A., Suzuki, K., Wechser, M., Goodsaid, F. & Caligiuri, M. A. ( 1999; ). Differential cytokine and chemokine gene expression by human NK cells following activation with IL-18 or IL-15 in combination with IL-12: implications for the innate immune response. J Immunol 162, 4511–4520.
    [Google Scholar]
  16. Ferlazzo, G., Pack, M., Thomas, D., Paludan, C., Schmid, D., Strowig, T., Bougras, G., Muller, W. A., Moretta, L. & Munz, C. ( 2004; ). Distinct roles of IL-12 and IL-15 in human natural killer cell activation by dendritic cells from secondary lymphoid organs. Proc Natl Acad Sci U S A 101, 16606–16611.[CrossRef]
    [Google Scholar]
  17. Gonzalez, E., Kulkarni, H., Bolivar, H., Mangano, A., Sanchez, R., Catano, G., Nibbs, R. J., Freedman, B. I., Quinones, M. P. & other authors ( 2005; ). The influence of CCL3L1 gene-containing segmental duplications on HIV-1/AIDS susceptibility. Science 307, 1434–1440.[CrossRef]
    [Google Scholar]
  18. Gougeon, M. L., Garcia, S., Heeney, J., Tschopp, R., Lecoeur, H., Guetard, D., Rame, V., Dauguet, C. & Montagnier, L. ( 1993; ). Programmed cell death in AIDS-related HIV and SIV infections. AIDS Res Hum Retroviruses 9, 553–563.[CrossRef]
    [Google Scholar]
  19. Grabstein, K. H., Eisenman, J., Shanebeck, K., Rauch, C., Srinivasan, S., Fung, V., Beers, C., Richardson, J., Schoenborn, M. A. & other authors ( 1994; ). Cloning of a T cell growth factor that interacts with the β chain of the interleukin-2 receptor. Science 264, 965–968.[CrossRef]
    [Google Scholar]
  20. Heeney, J., Jonker, R., Koornstra, W., Dubbes, R., Niphuis, H., Di Rienzo, A. M., Gougeon, M. L. & Montagnier, L. ( 1993; ). The resistance of HIV-infected chimpanzees to progression to AIDS correlates with absence of HIV-related T-cell dysfunction. J Med Primatol 22, 194–200.
    [Google Scholar]
  21. Ibegbu, C., Brodie-Hill, A., Kourtis, A. P., Carter, A., McClure, H., Wei Chen, Z. & Nahmias, A. J. ( 2001; ). Use of human CD3 monoclonal antibody for accurate CD4+ and CD8+ lymphocyte determinations in macaques: phenotypic characterization of the CD3− CD8+ cell subset. J Med Primatol 30, 291–298.[CrossRef]
    [Google Scholar]
  22. Kennedy, M. K., Glaccum, M., Brown, S. N., Butz, E. A., Viney, J. L., Embers, M., Matsuki, N., Charrier, K., Sedger, L. & other authors ( 2000; ). Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J Exp Med 191, 771–780.[CrossRef]
    [Google Scholar]
  23. Kestens, L., Vingerhoets, J., Peeters, M., Vanham, G., Vereecken, C., Penne, G., Niphuis, H., van Eerd, P., van der Groen, G. & other authors ( 1995; ). Phenotypic and functional parameters of cellular immunity in a chimpanzee with a naturally acquired simian immunodeficiency virus infection. J Infect Dis 172, 957–963.[CrossRef]
    [Google Scholar]
  24. Kottilil, S., Chun, T. W., Moir, S., Liu, S., McLaughlin, M., Hallahan, C. W., Maldarelli, F., Corey, L. & Fauci, A. S. ( 2003; ). Innate immunity in human immunodeficiency virus infection: effect of viremia on natural killer cell function. J Infect Dis 187, 1038–1045.[CrossRef]
    [Google Scholar]
  25. Kuniyoshi, J. S., Kuniyoshi, C. J., Lim, A. M., Wang, F. Y., Bade, E. R., Lau, R., Thomas, E. K. & Weber, J. S. ( 1999; ). Dendritic cell secretion of IL-15 is induced by recombinant huCD40LT and augments the stimulation of antigen-specific cytolytic T cells. Cell Immunol 193, 48–58.[CrossRef]
    [Google Scholar]
  26. Lauw, F. N., Dekkers, P. E. P., te Velde, A. A., Speelman, P., Levi, M., Kurimoto, M., Hack, C. E., van Deventer, S. J. H. & van der Poll, T. ( 1999; ). Interleukin-12 induces sustained activation of multiple host inflammatory mediator systems in chimpanzees. J Infect Dis 179, 646–652.[CrossRef]
    [Google Scholar]
  27. Lodolce, J., Burkett, P., Koka, R., Boone, D., Chien, M., Chan, F., Madonia, M., Chai, S. & Ma, A. ( 2002; ). Interleukin-15 and the regulation of lymphoid homeostasis. Mol Immunol 39, 537–544.[CrossRef]
    [Google Scholar]
  28. Matano, T., Shibata, R., Siemon, C., Connors, M., Lane, H. C. & Martin, M. A. ( 1998; ). Administration of an anti-CD8 monoclonal antibody interferes with the clearance of chimeric simian/human immunodeficiency virus during primary infections of rhesus macaques. J Virol 72, 164–169.
    [Google Scholar]
  29. Mueller, Y. M., Petrovas, C., Bojczuk, P. M., Dimitriou, I. D., Beer, B., Silvera, P., Villinger, F., Cairns, J. S., Gracely, E. J. & other authors ( 2005; ). Interleukin-15 increases effector memory CD8+ T cells and NK cells in simian immunodeficiency virus-infected macaques. J Virol 79, 4877–4885.[CrossRef]
    [Google Scholar]
  30. Musso, T., Calosso, L., Zucca, M., Millesimo, M., Ravarino, D., Giovarelli, M., Malavasi, F., Ponzi, A. N., Paus, R. & Bulfone-Paus, S. ( 1999; ). Human monocytes constitutively express membrane-bound, biologically active, and interferon-upregulated interleukin-15. Blood 93, 3531–3539.
    [Google Scholar]
  31. Neely, G. G., Epelman, S., Ma, L. L., Colarusso, P., Howlett, C. J., Amankwah, E. K., McIntyre, A. C., Robbins, S. M. & Mody, C. H. ( 2004; ). Monocyte surface-bound IL-15 can function as an activating receptor and participate in reverse signaling. J Immunol 172, 4225–4234.[CrossRef]
    [Google Scholar]
  32. Nehete, P. N., Schapiro, S. F., Johnson, P. C., Murthy, K. K., Satterfield, W. C. & Sastry, K. J. ( 1998; ). A synthetic peptide from the first conserved region in the envelope protein gp160 is a strong T-cell epitope in HIV-infected chimpanzees and humans. Viral Immunol 11, 147–158.[CrossRef]
    [Google Scholar]
  33. Neri, S., Mariani, E., Meneghetti, A., Cattini, L. & Facchini, A. ( 2001; ). Calcein-acetyoxymethyl cytotoxicity assay: standardization of a method allowing additional analyses on recovered effector cells and supernatants. Clin Diagn Lab Immunol 8, 1131–1135.
    [Google Scholar]
  34. Novembre, F. J., Saucier, M., Anderson, D. C., Klumpp, S. A., O'Neil, S. P., Brown, C. R., Hart, C. E., Guenthner, P. C., Swenson, R. B. & McClure, H. M. ( 1997; ). Development of AIDS in a chimpanzee infected with human immunodeficiency virus type 1. J Virol 71, 4086–4091.
    [Google Scholar]
  35. Obata-Onai, A., Hashimoto, S., Onai, N., Kurachi, M., Nagai, S., Shizuno, K., Nagahata, T. & Matsushima, K. ( 2002; ). Comprehensive gene expression analysis of human NK cells and CD8+ T lymphocytes. Int Immunol 14, 1085–1098.[CrossRef]
    [Google Scholar]
  36. Ogg, G. S., Kostense, S., Klein, M. R., Jurriaans, S., Hamann, D., McMichael, A. J. & Miedema, F. ( 1999; ). Longitudinal phenotypic analysis of human immunodeficiency virus type 1-specific cytotoxic T lymphocytes: correlation with disease progression. J Virol 73, 9153–9160.
    [Google Scholar]
  37. Ohteki, T., Suzue, K., Maki, C., Ota, T. & Koyasu, S. ( 2001; ). Critical role of IL-15-IL-15R for antigen-presenting cell functions in the innate immune response. Nat Immunol 2, 1138–1143.[CrossRef]
    [Google Scholar]
  38. Ondoa, P., Vingerhoets, J., Vereecken, C., Van Der Groen, G., Heeney, J. L. & Kestens, L. ( 2002; ). In vitro replication of SIVcpz is suppressed by β-chemokines and CD8+ T cells but not by natural killer cells of infected chimpanzees. AIDS Res Hum Retroviruses 18, 373–382.[CrossRef]
    [Google Scholar]
  39. Ondoa, P., Vereecken, C., Fransen, K., Colebunders, R., van der Groen, G., Heeney, J. L. & Kestens, L. ( 2003; ). Human and simian immunodeficiency virus-infected chimpanzees do not have increased intracellular levels of β-chemokines in contrast to infected humans. J Med Virol 69, 297–305.[CrossRef]
    [Google Scholar]
  40. O'Neil, S. P., Novembre, F. J., Hill, A. B., Suwyn, C., Hart, C. E., Evans-Strickfaden, T., Anderson, D. C., deRosayro, J., Herndon, J. G. & other authors ( 2000; ). Progressive infection in a subset of HIV-1 positive chimpanzees. J Infect Dis 182, 1051–1062.[CrossRef]
    [Google Scholar]
  41. Palmer, S., Wiegand, A. P., Maldarelli, F., Bazmi, H., Mican, J. M., Polis, M., Dewar, R. L., Planta, A., Liu, S. & other authors ( 2003; ). New real-time reverse transcriptase-initiated PCR assay with single-copy sensitivity for human immunodeficiency virus type 1 RNA in plasma. J Clin Microbiol 41, 4531–4536.[CrossRef]
    [Google Scholar]
  42. Pien, G. C., Satoskar, A. R., Takeda, K., Akira, S. & Biron, C. A. ( 2000; ). Selective IL-18 requirements for induction of compartmental IFN-γ responses during viral infection. J Immunol 165, 4787–4791.[CrossRef]
    [Google Scholar]
  43. Ranson, T., Vosshenrich, C. A., Corcuff, E., Richard, O., Laloux, V., Lehuen, A. & Di Santo, J. P. ( 2003; ). IL-15 is an essential mediator of peripheral NK-cell homeostasis. Blood 101, 4887–4893.[CrossRef]
    [Google Scholar]
  44. Sanders-Buell, E., Salminen, M. O. & McCutchan, F. E. ( 1995; ). Sequencing primers for HIV-1. Rockville, MD: Henry M. Jackson Foundation Research Laboratory and Division of Retrovirology, Walter Reed Army Institute of Research. http://hiv-web.lanl.gov/content/hiv-db/COMPENDIUM/1995/PART-III/3.pdf
  45. Schmidt, K. N., Leung, B., Kwong, M., Zarember, K. A., Satyal, S., Navas, T. A., Wang, F. & Godowski, P. J. ( 2004; ). APC-independent activation of NK cells by the toll-like receptor 3 agonist double-stranded RNA. J Immunol 172, 138–143.[CrossRef]
    [Google Scholar]
  46. Shu, U., Kiniwa, M., Wu, C. Y., Maliszewski, C., Vezzio, N., Hakimi, J., Gately, M. & Delespesse, G. ( 1995; ). Activated T cells induce interleukin-12 production by monocytes via CD40−CD40 ligand interaction. Eur J Immunol 25, 1125–1128.[CrossRef]
    [Google Scholar]
  47. Siren, J., Sareneva, T., Pirhonen, J., Strengell, M., Veckman, V., Julkunen, I. & Matikainen, S. ( 2004; ). Cytokine and contact-dependent activation of natural killer cells by influenza A or Sendai virus-infected macrophages. J Gen Virol 85, 2357–2364.[CrossRef]
    [Google Scholar]
  48. Skov, S., Bonyhadi, M., Odum, N. & Ledbetter, J. A. ( 2000; ). IL-2 and IL-15 regulate CD154 expression on activated CD4 T cells. J Immunol 164, 3500–3505.[CrossRef]
    [Google Scholar]
  49. 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-gamma production in human NK and T cells. J Immunol 170, 5464–5469.[CrossRef]
    [Google Scholar]
  50. ten Haaft, P., Murthy, K., Salas, M., McClure, H., Dubbes, R., Koornstra, W., Niphuis, H., Davis, D., van der Groen, G. & Heeney, J. ( 2001; ). Differences in early virus loads with different phenotypic variants of HIV-1 and SIVcpz in chimpanzees. AIDS 15, 2085–2092.[CrossRef]
    [Google Scholar]
  51. Vankayalapati, R., Kulcar, P., Wizel, B., Weis, S. E., Samten, B., Safi, H., Shams, H. & Barnes, P. F. ( 2004; ). NK cells regulate CD8+ T cell effector function in response to an intracellular pathogen. J Immunol 172, 130–137.[CrossRef]
    [Google Scholar]
  52. Vitale, M., Caruso, A., Licenziati, S., Rodella, L., Fiorentini, S., Zauli, G., Castelli, F., Manzoli, F. A. & Turano, A. ( 2000; ). Differential production of IFN-γ, analyzed at the single-cell level, by specific subsets of human NK and T cells from healthy and HIV+ subjects. Cytometry 39, 189–194.[CrossRef]
    [Google Scholar]
  53. Voevodin, A., Samilchuk, E. & Dashti, S. ( 1998; ). A survey for 32 nucleotide deletion in the CCR-5 chemokine receptor gene (deltaccr-5) conferring resistance to human immunodeficiency virus type 1 in different ethnic groups and in chimpanzees. J Med Virol 55, 147–151.[CrossRef]
    [Google Scholar]
  54. Waldmann, T. A. & Tagaya, Y. ( 1999; ). The multifaceted regulation of interleukin-15 expression and the role of this cytokine in NK cell differentiation and host response to intracellular pathogens. Annu Rev Immunol 17, 19–49.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.82154-0
Loading
/content/journal/jgv/10.1099/vir.0.82154-0
Loading

Data & Media loading...

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error