CpG-C immunostimulatory oligodeoxyribonucleotide activation of plasmacytoid dendritic cells in rhesus macaques to augment the activation of IFN-γ-secreting simian immunodeficiency virus-specific T cells

Journal of Immunology

Volumn 173, Issue 3, 2004, Pages 1647-1657

  Teleshova, Natalia ^a   Kenney, Jessica ^a   Jones, Jennifer ^a,f   Marshall, Jason ^b   Van Nest, Gary ^b   Dufour, Jason ^c   Bohm, Rudolf ^c   Lifson, Jeffrey D ^d   Gettie, Agegnehu ^e   Pope, Melissa ^a  

^a POPULATION COUNCIL   (United States)

^b Dynavax Technologies Corporation   (United States)

^c TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

^d SAIC FREDERICK INC   (United States)

^e AARON DIAMOND AIDS RESEARCH CENTER   (United States)

^f and Clinical Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; CD123 ANTIGEN; CD40 LIGAND; CD86 ANTIGEN; GAMMA INTERFERON; GLYCOPROTEIN P 15095; HLA DR ANTIGEN; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; INTERLEUKIN 12; INTERLEUKIN 3; OLIGODEOXYRIBONUCLEOTIDE; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; BONE MARROW CELL; CELL SUBPOPULATION; CONTROLLED STUDY; CPG ISLAND; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; DRUG EFFICACY; FEMALE; IMMUNITY; IMMUNOSTIMULATION; MALE; NONHUMAN; PRIORITY JOURNAL; RHESUS MONKEY; SIMIAN IMMUNODEFICIENCY VIRUS; T LYMPHOCYTE ACTIVATION;

EID: 3242749617     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.173.3.1647     Document Type: Article

References (85)

1. Liu, Y. J. 2001. Dendritic cell subsets and lineages, and their functions in innate and adaptive immunity. Cell 106:259.
2. Liu, Y. J., H. Kanzler, V. Soumelis, and M. Gilliet. 2001. Dendritic cell lineage, plasticity and cross-regulation. Nat. Immunol. 2:585.
3. Siegal, F. P., N. Kadowaki, M. Shodell, P. A. Fitzgerald-Bocarsly, K. Shah, S. Ho, S. Antonenko, and Y. J. Liu. 1999. The nature of the principal type 1 interferon-producing cells in human blood. Science 284:1835.
4. Cella, M., D. Jarrossay, F. Facchetti, O. Alebardi, H. Nakajima, A. Lanzavecchia, and M. Colonna. 1999. Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat. Med. 5:919.
5. Banchereau, J., and R. M. Steinman. 1998. Dendritic cells and the control of immunity. Nature 392:245.
6. 2, promote type 2 cytokine production in maturing human naive T helper cells. J. Immunol. 159:28.
7. Rissoan, M. C., V. Soumelis, N. Kadowaki, G. Grouard, F. Briere, R. de Waal Malefyt, and Y. J. Liu. 1999. Reciprocal control of T helper cell and dendritic cell differentiation. Science 283:1183.
8. - subclasses of dendritic cells direct the development of distinct T helper cells in vivo. J. Exp. Med. 189:587.
9. Kadowaki, N., S. Antoneko, J. Y.-N. Lau, and Y.-J. Liu. 2000. Natural interferon-α/β-producing cells link innate and adaptive immunity. J. Exp. Med. 192:219.
10. Bosio, C. M., M. J. Aman, C. Grogan, R. Hogan, G. Ruthel, D. Negley, M. Mohamadzadeh, S. Bavari, and A. Schmaljohn. 2003. Ebola and Marburg viruses replicate in monocyte-derived dendritic cells without inducing the production of cytokines and full maturation. J. Infect. Dis. 188:1630.
11. Tortorella, D., B. E. Gewurz, M. H. Furman, D. J. Schust, and H. L. Ploegh. 2000. Viral subversion of the immune system. Annu. Rev. Immunol. 18:861.
12. Engelmayer, J., M. Larsson, M. Subklewe, A. Chahroudi, A. Schmaljohn, C. William, R. M. Steinman, and N. Bhardwaj. 1999. Vaccinia virus inhibits the maturation of human dendritic cells: a novel mechanism of immune evasion. J. Immunol. 163:6762.
13. 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.
14. Yamamoto, J. K., F. Barre-Sinoussi, V. Bolton, N. C. Pedersen, and M. B. Gardner. 1986. Human α- and β-interferon but not γ- suppress the in vitro replication of LAV, HTLV-III, and ARV-2. J. Interferon Res. 6:143.
15. Hartshorn, K. L., D. Neumeyer, M. W. Vogt, R. T. Schooley, and M. S. Hirsch. 1987. Activity of interferons α, β, and γ against human immunodeficiency virus replication in vitro. AIDS Res. Hum. Retroviruses 3:125.
16. Poli, G., J. M. Orenstein, A. Kinter, T. M. Folks, and A. S. Fauci. 1989. Interferon-α but not AZT suppresses HIV expression in chronically infected cell lines. Science 244:575.
17. Biron, C. A. 1997. Activation and function of natural killer cell responses during viral infections. Curr. Opin. Immunol. 9:24.
18. Sun, S., X. Zhang, D. F. Tough, and J. Sprent. 1998. Type I interferon-mediated stimulation of T cells by CpG DNA. J. Exp. Med. 188:2335.
19. + T lymphocytes. J. Immunol. 164:6435.
20. Santini, S. M., T. Di Pucchio, C. Lapenta, S. Parlato, M. Logozzi, and F. Belardelli. 2003. A new type I IFN-mediated pathway for the rapid differentiation of monocytes into highly active dendritic cells. Stem Cells 21:357.
21. Carbonneil, C., A. Aouba, M. Burgard, S. Cardinaud, C. Rouzioux, P. Langlade-Demoyen, and L. Weiss. 2003. Dendritic cells generated in the presence of granulocyte-macrophage colony-stimulating factor and IFN-α are potent inducers of HIV-specific CD8 T cells. AIDS 17:1731.
22. Mattei, F., G. Schiavoni, F. Belardelli, and D. F. Tough. 2001. IL-15 is expressed by dendritic cells in response to type I IFN, double-stranded RNA, or lipopolysaccharide and promotes dendritic cell activation. J. Immunol. 167:1179.
23. Luft, T., P. Luetjens, H. Hochrein, T. Toy, K. A. Masterman, M. Rizkalla, C. Maliszewski, K. Shortman, J. Cebon, and E. Maraskovsky. 2002. IFN-α enhances CD40 ligand-mediated activation of immature monocyte-derived dendritic cells. Int. Immunol. 14:367.
24. Wiesemann, E., D. Sonmez, F. Heidenreich, and A. Windhagen. 2002. Interferon-β increases the stimulatory capacity of monocyte-derived dendritic cells to induce IL-13, IL-5 and IL-10 in autologous T-cells. J. Neuroimmunol. 123:160.
25. Santini, S. M., C. Lapenta, M. Logozzi, S. Parlato, M. Spada, T. Di Pucchio, and F. Belardelli. 2000. Type I Interferon as a powerful adjuvant for monocyte-derived dendritic cell development and activity in vitro and in Hu-PBL-SCID mice. J. Exp. Med. 191:1777.
26. Fonteneau, J. F., M. Larsson, A. S. Beignon, K. McKenna, I. Dasilva, A. Amara, Y. J. Liu, J. D. Lifson, D. R. Littman, and N. Bhardwaj. 2004. Human immunodeficiency virus type 1 activates plasmacytoid dendritic cells and concomitantly induces the bystander maturation of myeloid dendritic cells. J. Virol. 78:5223.
27. Patterson, S., A. Rae, N. Hockey, J. Gilmour, and F. Gotch. 2001. Plasmacytoid dendritic cells are highly susceptible to human immunodeficiency virus type 1 infection and release infectious virus. J. Virol. 75:6710.
28. - plasmacytoid dendritic cells in patients with HIV-1 infection correlates with HIV-1 RNA virus load. Blood 98:2574.
29. 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.
30. Macatonia, S. E., R. Lau, S. Patterson, A. J. Pinching, and S. C. Knight. 1990. Dendritic cell infection, depletion and dysfunction in HIV infected individuals. Immunology 71:38.
31. + (myeloid) dendritic cell numbers in primary HIV-1 infection. Blood 98:3016.
32. Grassi, F., A. Hosmalin, D. McIlroy, V. Calvez, P. Debre, and B. Autran. 1999. Depletion in blood CD11c-positive dendritic cells from HIV-infected patients. AIDS 13:759.
33. 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.
34. Moir, S., A. Malaspina, K. M. Ogwaro, E. T. Donoghue, C. W. Hallahan, L. A. Ehler, S. Liu, J. Adelsberger, R. Lapointe, P. Hwu, et al. 2001. HIV-1 induces phenotypic and functional perturbations of B cells in chronically infected individuals. Proc. Natl. Acad. Sci. USA 98:10362.
35. Rich, E. A., Z. Toossi, H. Fujiwara, R. Hanigosky, M. M. Lederman, and J. J. Ellner. 1988. Defective accessory function of monocytes in human immunodeficiency virus-related disease syndromes. J. Lab. Clin. Med. 112:174.
36. Krieg, A. M. 2002. CpG motifs in bacterial DNA and their immune effects. Annu. Rev. Immunol. 20:709.
37. Gursel, M., D. Verthelyi, and D. M. Klinman. 2002. CpG oligodeoxynucleotides induce human monocytes to mature into functional dendritic cells. Eur. J. Immunol. 32:2617.
38. Krug, A., A. Towarowski, S. Britsch, S. Rothenfusser, V. Hornung, R. Bals, T. Giese, H. Engelmann, S. Endres, A. M. Krieg, and G. Hartmann. 2001. Toll-like receptor expression reveals CpG DNA as a unique microbial stimulus for plasmacytoid dendritic cells which synergizes with CD40 ligand to induce high amounts of IL-12. Eur. J. Immunol. 31:3026.
39. Marshall, J. D., K. Fearon, C. Abbate, S. Subramanian, P. Yee, J. Gregorio, R. L. Coffman, and G. Van Nest. 2003. Identification of a novel CpG DNA class and motif that optimally stimulate B cell and plasmacytoid dendritic cell functions. J. Leukocyte Biol. 73:781.
40. Hartmann, G., J. Battiany, H. Poeck, M. Wagner, M. Kerkmann, N. Lubenow, S. Rothenfusser, and S. Endres. 2003. Rational design of new CpG oligonucleotides that combine B cell activation with high IFN-α induction in plasmacytoid dendritic cells. Eur. J. Immunol. 33:1633.
41. Desrosiers, R. C. 1990. The simian immunodeficiency viruses. Annu. Rev. Immunol. 8:557.
42. O'Doherty, U., R. Ignatius, N. Bhardwaj, and M. Pope. 1997. Generation of monocyte-derived cells from the precursors in rhesus macaque blood. J. Immunol. Methods 207:185.
43. Pope, M., D. Elmore, D. Ho, and P. Marx. 1997. Dendritic cell-T cell mixtures, isolated from the skin and mucosae of macaques, support the replication of SIV. AIDS Res. Hum. Retroviruses 13:819.
44. Mehlhop, E. R., L. A. Villamide, I. Frank, A. Gettie, C. Santisteban, D. Messmer, R. Ignatius, J. D. Lifson, and M. Pope. 2002. Enhanced in vitro stimulation of rhesus macaque dendritic cells for activation of SIV-specific T cell responses. J. Immunol. Methods 260:219.
45. Barratt-Boyes, S. M., M. I. Zimmer, L. A. Harshyne, E. M. Meyer, S. C. Watkins, S. Capuano, III, M. Murphey-Corb, L. D. Falo, Jr., and A. D. Donnenberg. 2000. Maturation and trafficking of monocyte-derived dendritic cells in monkeys: implications for dendritic cell-based vaccines. J. Immunol. 164:2487.
46. Coates, P. T., S. M. Barratt-Boyes, L. Zhang, V. S. Donnenberg, P. J. O'Connell, A. J. Logar, F. J. Duncan, M. Murphey-Corb, A. D. Donnenberg, A. E. Morelli, et al. 2003. Dendritic cell subsets in blood and lymphoid tissue of rhesus monkeys and their mobilization with Flt3 ligand. Blood 102:2513.
47. Pichyangkul, S., T. P. Endy, S. Kalayanarooj, A. Nisalak, K. Yongvanitchit, S. Green, A. L. Rothman, F. A. Ennis, and D. H. Libraty. 2003. A blunted blood plasmacytoid dendritic cell response to an acute systemic viral infection is associated with increased disease severity. J. Immunol. 171:5571.
48. Teleshova, N., J. Jones, J. Kenney, J. Purcell, R. Bohm, A. Gettie, and M. Pope. 2004. Short-term Flt3L treatment effectively mobilizes macaque myeloid dendritic cells. J. Leukocyte Biol. 75:1102.
49. Frank, I., M. J. Piatak, H. Stoessel, N. Romani, D. Bonnyay, J. D. Lifson, and M. Pope. 2002. Infectious and whole inactivated simian immunodeficiency viruses interact similarly with primate dendritic cells (DCs): Differential intracellular fate of virions in mature and immature DCs. J. Virol. 76:2936.
50. Turville, S. G., J. J. Santos, I. Frank, P. U. Cameron, J. Wilkinson, M. Miranda-Saksena, J. Dable, H. Stoessel, N. Romani, M. Piatak, et al. 2004. Immunodeficiency virus uptake, turnover and two phase transfer in human dendritic cells. Blood 103:2170.
51. + T cell responses. J. AIDS 34:7.
52. Larsson, M., J. F. Fonteneau, M. Lirvall, P. Haslett, J. D. Lifson, and N. Bhardwaj. 2002. Activation of HIV-1 specific CD4 and CD8 T cells by human dendritic cells: roles for cross-presentation and non-infectious HIV-1 virus. AIDS 16:1319.
53. Moris, A., C. Nobile, F. Buseyne, F. Porrot, J.-P. Abastado, and O. Schwartz. 2004. DC-SIGN promotes exogenous MHC-I restricted HIV-1 antigen presentation. Blood 103:2648.
54. Connor, R. I., D. C. Montefiori, J. M. Binley, J. P. Moore, S. Bonhoeffer, A. Gettie, E. A. Fenamore, K. E. Sheridan, D. D. Ho, P. J. Dailey, and P. A. Marx. 1998. Temporal analyses of virus replication, immune responses, and efficacy in rhesus macaques immunized with a live, attenuated simian immunodeficiency virus vaccine. J. Virol. 72:7501.
55. Ignatius, R., K. Tenner-Racz, D. Messmer, A. Gettie, A. Luckay, C. Russo, S. Smith, P. A. Marx, R. M. Steinman, P. Racz, and M. Pope. 2002. Increased macrophage infection upon subcutaneous inoculation of rhesus macaques with simian immunodeficiency virus-loaded dendritic cells or T cells but not with cell-free virus. J. Virol. 76:9787.
56. Hu, J., M. Pope, U. O'Doherty, C. Brown, and C. J. Miller. 1998. Immunophenotypic characterization of SIV-infected cells in cervix, vagina and draining lymph nodes of chronically infected rhesus macaques. Lab. Invest. 78:435.
57. Hu, J., C. J. Miller, U. O'Doherty, P. A. Marx, and M. Pope. 1999. The dendritic cell-T cell milieu of the lymphoid tissue of the tonsil provides a locale in which SIV can reside and propagate at chronic stages of infection. AIDS Res. Hum. Retroviruses 15:1305.
58. Chertova, E., J. W. Bess Jr., B. J. Crise, R. C. Sowder II, T. M. Schaden, J. M. Hilburn, J. A. Hoxie, R. E. Benveniste, J. D. Lifson, L. E. Henderson, and L. O. Arthur. 2002. Envelope glycoprotein incorporation, not shedding of surface envelope glycoprotein (gp120/SU), is the primary determinant of SU content of purified human immunodeficiency virus type 1 and simian immunodeficiency virus. J. Virol. 76:5315.
59. + lymphocytes in control of simian immunodeficiency virus infection and resistance to rechallenge after transient early antiretroviral treatment. J. Virol. 75:10187.
60. Grouard, G., M.-C. Rissoan, L. Filgueira, I. Durand, J. Banchereau, and Y.-J. Liu. 1997. The enigmatic plasmacytoid T cells develop into dendritic cells with IL-3 and CD40-ligand. J. Exp. Med. 185:1101.
61. Olweus, J., A. BitMansour, R. Warnke, P. A. Thompson, J. Carballido, L. J. Picker, and F. Lund-Johansen. 1997. Dendritic cell ontogeny: a human cell lineage of myeloid origin. Proc. Natl. Acad. Sci. USA 94:12551.
62. O'Doherty, U., M. Peng, S. Gezelter, W. J. Swiggard, M. Betjes, N. Bhardwaj, and R. M. Steinman. 1994. Human blood contains two subsets of dendritic cells, one immunologically mature, and the other immature. Immunology 82:487.
63. O'Doherty, U., R. M. Steinman, M. Peng, P. U. Cameron, S. Gezelter, I. Kopeloff, W. J. Swiggard, M. Pope, and N. Bhardwaj. 1993. Dendritic cells freshly isolated from human blood express CD4 and mature into typical immunostimulatory dendritic cells after culture in monocyte-conditioned medium. J. Exp. Med. 178:1067.
64. Duramad, O., K. L. Fearon, J. H. Chan, H. Kanzler, J. D. Marshall, R. L. Coffman, and F. J. Barrat. 2003. IL-10 regulates plasmacytoid dendritic cell response to CpG-containing immunostimulatory sequences. Blood 102:4487.
65. Klagge, I. M., V. ter Meulen, and S. Schneider-Schaulies. 2000. Measles virus-induced promotion of dendritic cell maturation by soluble mediators does not overcome the immunosuppressive activity of viral glycoproteins on the cell surface. Eur. J. Immunol. 30:2741.
66. Ghanekar, S., L. Zheng, A. Logar, J. Navratil, L. Borowski, P. Gupta, and C. Rinaldo. 1996. Cytokine expression by human peripheral blood dendritic cells stimulated in vitro with HIV-1 and herpes simplex virus. J. Immunol. 157:4028.
67. Cella, M., M. Salio, Y. Sakakibara, H. Langen, I. Julkunen, and A. Lanzavecchia. 1999. Maturation, activation, and protection of dendritic cells induced by double-stranded RNA. J. Exp. Med. 189:821.
68. Thomas, R., L. S. Davis, and P. E. Lipsky. 1993. Isolation and characterization of human peripheral blood dendritic cells. J. Immunol. 150:821.
69. McLellan, A. D., G. C. Starling, L. A. Williams, B. D. Hock, and D. N. J. Hart. 1995. Activation of human peripheral blood dendritic cells induces the CD86 co-stimulatory molecule, Eur. J. Immunol. 25:2064.
70. Pierre, P., S. J. Turley, E. Gatti, M. Hull, J. Meltzer, A. Mirza, K. Inaba, R. M. Steinman, and I. Mellman. 1997. Developmental regulation of MHC class II transport in mouse dendritic cells. Nature 388:787.
71. Clatza, A., L. C. Bonifaz, D. A. Vignali, and J. Moreno. 2003. CD40-induced aggregation of MHC class II and CD80 on the cell surface leads to an early enhancement in antigen presentation. J. Immunol. 171:6478.
72. Kelsall, B. L., E. Stuber, M. Neurath, and W. Strober. 1996. Interleukin-12 production by dendritic cells: the role of CD40-CD40L interactions in Th1 T-cell responses. Ann. NY Acad. Sci. 795:116.
73. Peng, X., A. Kasran, P. A. Warmerdam, M. de Boer, and J. L. Ceuppens. 1996. Accessory signaling by CD40 for T cell activation: induction of Th1 and Th2 cytokines and synergy with interleukin-12 for interferon-γ production. Eur. J. Immunol. 26:1621.
74. Gibson, S. J., J. M. Lindh, T. R. Riter, R. M. Gleason, L. M. Rogers, A. E. Fuller, J. L. Oesterich, K. B. Gorden, X. Qiu, S. W. McKane, et al. 2002. Plasmacytoid dendritic cells produce cytokines and mature in response to the TLR7 agonists, imiquimod and resiquimod. Cell. Immunol. 218:74.
75. Gary-Gouy, H., P. Lebon, and A. H. Dalloul. 2002. Type I interferon production by plasmacytoid dendritic cells and monocytes is triggered by viruses, but the level of production is controlled by distinct cytokines. J. Interferon Cytokine Res. 22:653.
76. Dumais, N., A. Patrick, R. B. Moss, H. L. Davis, and K. L. Rosenthal. 2002. Mucosal immunization with inactivated human immunodeficiency virus plus CpG oligodeoxynucleotides induces genital immune responses and protection against intravaginal challenge. J. Infect. Dis. 186:1098.
77. Anders, H. J., B. Banas, Y. Linde, L. Weller, C. D. Cohen, M. Kretzler, S. Martin, V. Vielhauer, D. Schlondorff, and H. J. Grone. 2003. Bacterial CpG-DNA aggravates immune complex glomerulonephritis: role of TLR9-mediated expression of chemokines and chemokine receptors. J. Am. Soc. Nephrol. 14:317.
78. Raghavan, S., J. Nystrom, M. Fredriksson, J. Holmgren, and A. M. Harandi. 2003. Orally administered CpG oligodeoxynucleotide induces production of CXC and CC chemokines in the gastric mucosa and suppresses bacterial colonization in a mouse model of Helicobacter pylori infection. Infect. Immun. 71:7014.
79. Soumelis, V., I. Scott, Y.-J. Liu, and J. Levy. 2002. Natural interferon-α producing cells in HIV infection. Hum. Immunol. 63:1206.
80. Willey, R. L., R. Byrum, M. Piatak, Y. B. Kim, M. W. Cho, J. L. Rossio, Jr., J. Bess, Jr., T. Igarishi, Y. Endo, L. O. Arthur, et al. 2003. Control of viremia and prevention of SHIV induced disease in rhesus macaques immunized with inactivated SIV and HIV-1 particles. J. Virol. 77:1163.
81. Lifson, J. D., M. Piatak, Jr., J. L. Rossio, J. Bess, Jr., E. Chertova, D. Schneider, R. Kiser, V. Coalter, B. Poore, R. Imming, et al. 2002. Whole inactivated SIV virion vaccines with functional envelope glycoproteins: safety, immunogenicity, and activity against intrarectal challenge. J. Med. Primatol. 31:205.
82. Teleshova, N., I. Frank, and M. Pope. 2003. Immunodeficiency virus exploitation of dendritic cells in the early steps of infection. J. Leukocyte Biol. 74:683.
83. Marrack, P., J. Kappler, and T. Mitchell. 1999. Type I interferons keep activated T cells alive. J. Exp. Med. 189:521.
84. Matikainen, S., T. Sareneva, T. Ronni, A. Lehtonen, P. J. Koskinen, and I. Julkunen. 1999. Interferon-α activates multiple STAT proteins and upregulates proliferation-associated IL-2Rα, c-myc, and pim-1 genes in human T cells. Blood 93:1980.
85. Su, L., and M. David. 1999. Inhibition of B cell receptor-mediated apoptosis by IFN. J. Immunol. 162:6317.