TLR ligand-dependent activation of naive CD4 T cells by plasmacytoid dendritic cells is impaired in hepatitis C virus infection

Journal of Immunology

Volumn 178, Issue 7, 2007, Pages 4436-4444

  Yonkers, Nicole L ^a   Rodriguez, Benigno ^a   Milkovich, Kimberly A ^a   Asaad, Robert ^a   Lederman, Michael M ^a   Heeger, Peter S ^b   Anthony, Donald D ^a,b,c  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

^c CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; CYTOKINE; GAMMA INTERFERON; HLA DR ANTIGEN; INTERLEUKIN 6; LIGAND; RECOMBINANT INTERLEUKIN 3; RECOMBINANT TUMOR NECROSIS FACTOR ALPHA; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9; VIRUS RNA;

ARTICLE; CD4+ T LYMPHOCYTE; CHRONIC HEPATITIS; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; FLOW CYTOMETRY; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; IMMUNE RESPONSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; VIRUS HEPATITIS;

EID: 33947661034     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.178.7.4436     Document Type: Article

References (53)

1. Freeman, A. J., G. J. Dore, M. G. Law, M. Thorpe, J. Von Overbeck, A. R. Lloyd, G. Marinos, and J. M. Kaldor. 2001. Estimating progression to cirrhosis in chronic hepatitis C virus infection. Hepatology 34: 809-816.
2. Lauer, G. M., and B. D. Walker. 2001. Hepatitis C virus infection. N. Engl. J. Med. 345: 41-52.
3. Valdez, H., D. Anthony, F. Farukhi, A. Patki, J. Salkowitz, P. Heeger, D. L. Peterson, A. B. Post, R. Asaad, and M. M. Lederman. 2000. Immune responses to hepatitis C and non-hepatitis C antigens in hepatitis C virus infected and HIV-1 coinfected patients. AIDS 14: 2239-2246.
4. Valdez, H., N. L. Carlson, A. B. Post, R. Asaad, P. S. Heeger, M. M. Lederman, P. V. Lehmann, and D. D. Anthony. 2002. HIV long-term non-progressors maintain brisk CD8 T cell responses to other viral antigens. AIDS 16: 1113-1111.
5. Nguyen, T. N., G. M. Lauer, R. T. Chung, and B. D. Walker. 2000. Cellular immune response in HIV/HCV co-infection. Hepatology 32: 270A.
6. + T lymphocytes after infection with hepatitis C virus. J. Virol. 75: 5550-5558.
7. + T cells in chronic hepatitis C virus infection. J. Immunol. 169: 3447-3458.
8. Keeffe, E. B., S. Iwarson, B. J. McMahon, K. L. Lindsay, R. S. Koff, M. Manns, R. Baumgarten, M. Wiese, M. Fourneau, A. Safary, et al. 1998. Safety and immunogenicity of hepatitis A vaccine in patients with chronic liver disease. Hepatology 27: 881-886.
9. Wedemeyer, H., C. Loos, J. Hadem, M. Bastuerk, M. Cornberg, B. Tegtmeyer, H. Liermann, N. Kezmic, H. L. Tillmann, and M. P. Manns. 2002. Impaired cellular immune response after influenza vaccination in patients with chronic hepatitis C infection. Hepatology 36: 276A.
10. Wiedmann, M., U. G. Liebert, U. Oesen, H. Porst, M. Wiese, S. Schroeder, U. Halm, J. Mossner, and F. Berr. 2000. Decreased immunogenicity of recombinant hepatitis B vaccine in chronic hepatitis C. Hepatology 31: 230-234.
11. Lanzavecchia, A., and F. Sallusto. 2001. The instructive role of dendritic cells on T cell responses; lineages, plasticity and kinetics. Curr. Opin. Immunol. 13: 291-298.
12. Banchereau, J., F. Briere, C. Caux, J. Davoust, S. Lebecque, Y. J. Liu, B. Pulendran, and K. Palucka. 2000. Immunobiology of dendritic cells. Annu. Rev. Immunol. 18: 767-811.
13. 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: 1183-1186.
14. Adams, S., D. W. O'Neill, and N. Bhardwaj. 2005. Recent advances in dendritic cell biology. J. Clin. Immunol. 25: 87-98.
15. Liu, Y. J. 2005. IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu. Rev. Immunol. 23: 275-306.
16. McKenna, K., A. S. Beignon, and N. Bhardwaj. 2005. Plasmacytoid dendritic cells: linking innate and adaptive immunity. J. Virol. 79: 17-27.
17. Bowie, A. G., and I. R. Haga. 2005. The role of Toll-like receptors in the host response to viruses. Mol. Immunol. 42: 859-867.
18. Lore, K., M. R. Betts, J. M. Brenchley, J. Kuruppu, S. Khojasteh, S. Perfetto, M. Roederer, R. A. Seder, and R. A. Koup. 2003. Toll-like receptor ligands modulate dendritic cells to augment cytomegalovirus- and HIV-1-specific T cell responses. J. Immunol. 171: 4320-4328.
19. Anthony, D. D., N. L. Yonkers, A. B. Post, R. Asaad, F. P. Heinzel, M. M. Lederman, P. V. Lehmann, and H. Valdez. 2004. Selective impairments in dendritic cell associated function distinguish HCV and HIV infection. J. Immunol. 172: 4907-4916.
20. Szabo, G., and A. Dolganiuc. 2005. Subversion of plasmacytoid and myeloid dendritic cell functions in chronic HCV infection. Immunobiology 210: 237-247.
21. Ulsenheimer, A., J. T. Gerlach, M. C. Jung, N. Gruener, M. Wachtler, M. Backmund, T. Santantonio, W. Schraut, M. H. Heeg, C. A. Schirren, et al. 2005. Plasmacytoid dendritic cells in acute and chronic hepatitis C virus infection. Hepatology 41: 643-651.
22. Wertheimer, A. M., A. Bakke, and H. R. Rosen. 2004. Direct enumeration and functional assessment of circulating dendritic cells in patients with liver disease. Hepatology 40: 335-345.
23. Auffermann-Gretzinger, S., E. B. Keeffe, and S. Levy. 2001. Impaired dendritic cell maturation in patients with chronic, but not resolved, hepatitis C virus infection. Blood 97: 3171-3176.
24. Bain, C., A. Fatmi, F. Zoulim, J. P. Zarski, C. Trepo, and G. Inchauspe. 2001. Impaired allostimulatory function of dendritic cells in chronic hepatitis C infection. Gastroenterology 120: 512-524.
25. Kanto, T., N. Hayashi, T. Takehara, T. Tatsumi, N. Kuzushita, A. Ito, Y. Sasaki, A. Kasahara, and M. Hon. 1999. Impaired allostimulatory capacity of peripheral blood dendritic cells recovered from hepatitis C virus-infected individuals. J. Immunol. 162: 5584-5591.
26. Longman, R. S., A. H. Talal, I. M. Jacobson, M. L. Albert, and C. M. Rice. 2004. Presence of functional dendritic cells in patients chronically infected with hepatitis C virus. Blood 103: 1026-1029.
27. Rollier, C., J. A. Drexhage, B. E. Verstrepen, E. J. Verschoor, R. E. Bontrop, G. Koopman, and J. L. Heeney. 2003. Chronic hepatitis C virus infection established and maintained in chimpanzees independent of dendritic cell impairment. Hepatology 38: 851-858.
28. Goutagny, N., C. Vieux, E. Decullier, B. Ligeoix, A. Epstein, C. Trepo, P. Courigou, G. Inchauspe, and C. Bain. 2004. Quantification and functional analysis of plasmacytoid dendritic cells in patients with chronic hepatitis C virus infection. J. Infect. Dis. 189: 1646-1655.
29. Kanto, T., M. Inoue, H. Miyatake, A. Sato, M. Sakakibara, T. Yakushijin, C. Oki, I. Itose, N. Hiramatsu, T. Takehara, et al. 2004. Reduced numbers and impaired ability of myeloid and plasmacytoid dendritic cells to polarize T helper cells in chronic hepatitis C virus infection. J. Infect. Dis. 190: 1919-1926.
30. Anthony, D. D., A. B. Post, H. Valdez, D. L. Peterson, M. Murphy, and P. S. Heeger. 2001. ELISPOT analysis of hepatitis C virus protein-specific IFN-γ-producing peripheral blood lymphocytes in infected humans with and without cirrhosis. Clin. Immunol. 99: 232-240.
31. Karulin, A., M. Hesse, M. Tary-Lehmann, and P. Lehmann. 2000. Single-cytokine-producing CD4 memory cells predominate in type 1 and type 2 immunity. J. Immunol. 164: 1862-1872.
32. 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 interleukin (IL)-3 and CD40-ligand. J. Exp. Med. 185: 1101-1111.
33. 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: 487-493.
34. 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.
35. Piccioli, D., S. Tavarini, S. Nuti, P. Colombatto, M. Brunetto, F. Bonino, P. Ciccorossi, F. Zorat, G. Pozzato, C. Comar, et al. 2005. Comparable functions of plasmacytoid and monocyte-derived dendritic cells in chronic hepatitis C patients and healthy donors. J. Hepatol. 42: 61-67.
36. Longman, R. S., A. H. Talal, I. M. Jacobson, C. M. Rice, and M. L. Albert. 2005. Normal functional capacity in circulating myeloid and plasmacytoid dendritic cells in patients with chronic hepatitis C. J. Infect. Dis. 192: 497-503.
37. Dolganiuc, A., S. Chang, K. Kodys, P. Mandrekar, G. Bakis, M. Cormier, and G. Szabo. 2006. Hepatitis C virus (HCV) core protein-induced, monocyte-mediated mechanisms of reduced IFN-α and plasmacytoid dendritic cell loss in chronic HCV infection. J. Immunol. 177: 6758-6768.
38. + T cells by dendritic cells expressing hepatitis C virus core and E1 proteins. J. Virol. 76: 5062-5070.
39. Dolganiuc, A., K. Kodys, A. Kopasz, C. Marshall, T. Do, L. Romics, Jr., P. Mandrekar, M. Zapp, and G. Szabo. 2003. Hepatitis C virus core and non-structural protein 3 proteins induce pro- and anti-inflammatory cytokines and inhibit dendritic cell differentiation. J. Immunol. 170: 5615-5624.
40. Dolganiuc, A., S. Oak, K. Kodys, D. T. Golenbock, R. W. Finberg, E. Kurt-Jones, and G. Szabo. 2004. Hepatitis C core and nonstructural 3 proteins trigger Toll-like receptor 2-mediated pathways and inflammatory activation. Gastroenterology 127: 1513-1524.
41. Kobayashi, K., L. D. Hernandez, J. E. Galan, C. A. Janeway, Jr., R. Medzhitov, and R. A. Flavell. 2002. IRAK-M is a negative regulator of Toll-like receptor signaling. Cell 110: 191-202.
42. Dobrovolskaia, M. A., A. E. Medvedev, K. E. Thomas, N. Cuesta, V. Toshchakov, T. Ren, M. J. Cody, S. M. Michalek, N. R. Rice, and S. N. Vogel. 2003. Induction of in vitro reprogramming by Toll-like receptor (TLR)2 and TLR4 agonists in murine macrophages: effects of TLR "homotolerance" versus "heterotolerance" on NF-κB signaling pathway components. J. Immunol. 170: 508-519.
43. Harte, M. T., I. R. Haga, G. Maloney, P. Gray, P. C. Reading, N. W. Bartlett, G. L. Smith, A. Bowie, and L. A. O'Neill. 2003. The poxvirus protein A52R targets Toll-like receptor signaling complexes to suppress host defense. J. Exp. Med. 197: 343-351.
44. Lechmann, M., S. Berchtold, J. Hauber, and A. Steinkasserer. 2002. CD83 on dendritic cells: more than just a marker for maturation. Trends Immunol. 23: 273-275.
45. 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: 861-926.
46. Palucka, K., and J. Banchereau. 2002. How dendritic cells and microbes interact to elicit or subvert protective immune responses. Curr. Opin. Immunol. 14: 420-431.
47. 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.
48. 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.
49. 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.
50. Mahanty, S., K. Hutchinson, S. Agarwal, M. McRae, P. E. Rollin, and B. Pulendran. 2003. Cutting edge: impairment of dendritic cells and adaptive immunity by Ebola and Lassa viruses. J. Immunol. 170: 2797-2801.
51. Kruse, M., O. Rosorius, F. Kratzer, G. Stelz, C. Kuhnt, G. Schuler, J. Hauber, and A. Steinkasserer. 2000. Mature dendritic cells infected with herpes simplex virus type 1 exhibit inhibited T-cell stimulatory capacity. J. Virol. 74: 7127-7136.
52. Fugier-Vivier, I., C. Servet-Delprat, P. Rivailler, M. C. Rissoan, Y. J. Liu, and C. Rabourdin-Combe. 1997. Measles virus suppresses cell-mediated immunity by interfering with the survival and functions of dendritic and T cells. J. Exp. Med. 186: 813-823.
53. Pichyangkul, S., T. P. Endy, S. Kalayanarooj, A. Nisalak, K. Yongvanitchit, S. Green, A. L. Rothman, F. A. Ennis, and D. H. Library. 2003. A blunted blood plasmacytoid dendritic cell response to an acute systemic viral infection is associated with increased disease severity. J. Immunol. 171: 5571-5578.