The potential use of Toll-like receptor agonists to restore the dysfunctional immunity induced by hepatitis C virus

Cellular Immunology

Volumn 262, Issue 2, 2010, Pages 96-104

  Salem, Mohamed L ^a,b   EL Demellawy, Maha ^c   El Azm, Abdel Raouf Abou ^d  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b Tanta University   (Egypt)

^c GENETIC ENGINEERING AND BIOTECHNOLOGY RESEARCH INSTITUTE   (Egypt)

^d TANTA UNIVERSITY   (Egypt)

Author keywords

Dendritic cells (DCs); Hepatitis C virus (HCV) infection; IFN ; Immune response; Immune therapy; Myeloid derived suppressor cells (MDSC); Natural killer (NK) cells; Regulatory T cells; Ribavirin therapy; TLR

Indexed keywords

ALANINE AMINOTRANSFERASE; ALPHA INTERFERON; AMPLIGEN; CPG OLIGODEOXYNUCLEOTIDE; CYCLOPHOSPHAMIDE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4 ANTIBODY; DACLIZUMAB; DENILEUKIN DIFTITOX; GAMMA INTERFERON; HEPATITIS C ANTIGEN; HEPATITIS C VACCINE; HILTONOL; IMIQUIMOD; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 10 ANTIBODY; INTERLEUKIN 12; INTERLEUKIN 6; ISATORIBINE; MONOCYTE CHEMOTACTIC PROTEIN 1; N METHYLTRYPTOPHAN; PEGINTERFERON ALPHA; POLYINOSINIC POLYCYTIDYLIC ACID; PROTEIN TYROSINE KINASE; RIBAVIRIN; SUNITINIB; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9; TOLL LIKE RECEPTOR AGONIST; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ADJUVANT THERAPY; CELL ACTIVATION; CYTOKINE RELEASE; DENDRITIC CELL; DRUG TREATMENT FAILURE; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; IMMUNE RESPONSE; INFECTION RESISTANCE; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PUBLIC HEALTH PROBLEM; REGULATORY T LYMPHOCYTE; REVIEW; SUPPRESSOR CELL; VIRUS IMMUNITY;

ADJUVANTS, IMMUNOLOGIC; ANTIVIRAL AGENTS; DENDRITIC CELLS; ENZYME INHIBITORS; HEPACIVIRUS; HEPATITIS C, CHRONIC; HUMANS; IMMUNITY, INNATE; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INTERFERON-ALPHA; KILLER CELLS, NATURAL; PROTEIN-TYROSINE KINASES; RIBAVIRIN; T-LYMPHOCYTES, REGULATORY; TOLL-LIKE RECEPTORS;

HEPATITIS C VIRUS;

EID: 77950859141     PISSN: 00088749     EISSN: 10902163     Source Type: Journal    
DOI: 10.1016/j.cellimm.2010.03.002     Document Type: Review

References (169)

1. Raza S.A., Clifford G.M., Franceschi S. Worldwide variation in the relative importance of hepatitis B and hepatitis C viruses in hepatocellular carcinoma: a systematic review. Br. J. Cancer 2007, 96:1127-1134.
2. Memon M.I., Memon M.A. Hepatitis C: an epidemiological review. J. Viral Hepat. 2002, 9:84-100.
3. Hepatitis E fact sheet (revised August 2004), Wkly. Epidemiol. Rec. 79 (2004) 314-316.
4. Lehman E.M., Wilson M.L. Epidemic hepatitis C virus infection in Egypt: estimates of past incidence and future morbidity and mortality. J. Viral Hepat. 2009, 16:650-658.
5. Paez Jimenez A., El-Din N.S., El-Hoseiny M., El-Daly M., Abdel-Hamid M., El Aidi S., Sultan Y., El-Sayed N., Mohamed M.K., Fontanet A. Community transmission of hepatitis B virus in Egypt: results from a case-control study in Greater Cairo. Int. J. Epidemiol. 2009, 38:757-765.
6. Kamal S.M. Acute hepatitis C: a systematic review. Am. J. Gastroenterol. 2008, 103:1283-1297. quiz 1298.
7. McHutchison J.G., Fried M.W. Current therapy for hepatitis C: pegylated interferon and ribavirin. Clin. Liver Dis. 2003, 7:149-161.
8. Hilleman M.R. Critical overview and outlook: pathogenesis, prevention, and treatment of hepatitis and hepatocarcinoma caused by hepatitis B virus. Vaccine 2003, 21:4626-4649.
9. Lin O.S., Keeffe E.B. Current treatment strategies for chronic hepatitis B and C. Annu. Rev. Med. 2001, 52:29-49.
10. Chang D.Y., Shin E.C. Immune-based therapy for chronic hepatitis C. J. Leukoc. Biol. 2009, 86:33-39.
11. Hepatitis C: global prevalence, Wkly. Epidemiol. Rec. 72 (1997) 341-344.
12. Singh R., Kaul R., Kaul A., Khan K. A comparative review of HLA associations with hepatitis B and C viral infections across global populations. World J. Gastroenterol. 2007, 13:1770-1787.
13. Armstrong G.L., Wasley A., Simard E.P., McQuillan G.M., Kuhnert W.L., Alter M.J. The prevalence of hepatitis C virus infection in the United States, 1999 through 2002. Ann. Intern. Med. 2006, 144:705-714.
14. Frank C., Mohamed M.K., Strickland G.T., Lavanchy D., Arthur R.R., Magder L.S., El Khoby T., Abdel-Wahab Y., Aly Ohn E.S., Anwar W., Sallam I. The role of parenteral antischistosomal therapy in the spread of hepatitis C virus in Egypt. Lancet 2000, 355:887-891.
15. Blackard J.T., Rouster S.D., Nady S., Galal G., Marzuuk N., Rafaat M.M., Daef E., El Din S.S., Purcell R.H., Emerson S.U., Sherman K.E., Shata M.T. Genotypic characterization of symptomatic hepatitis E virus (HEV) infections in Egypt. J. Clin. Virol. 2009.
16. El Awady M.K., Azzazy H.M., Fahmy A.M., Shawky S.M., Badreldin N.G., Yossef S.S., Omran M.H., Zekri A.R., Goueli S.A. Positional effect of mutations in 5'UTR of hepatitis C virus 4a on patients' response to therapy. World J. Gastroenterol. 2009, 15:1480-1486.
17. Ray S.C., Arthur R.R., Carella A., Bukh J., Thomas D.L. Genetic epidemiology of hepatitis C virus throughout egypt. J. Infect. Dis. 2000, 182:698-707.
18. Elrefaei M., El-sheikh N., Kamal K., Cao H. Analysis of T cell responses against hepatitis C virus genotype 4 in Egypt. J. Hepatol. 2004, 40:313-318.
19. Bowen D.G., Walker C.M. Adaptive immune responses in acute and chronic hepatitis C virus infection. Nature 2005, 436:946-952.
20. Aronsohn A., Reau N. Long-term outcomes after treatment with interferon and ribavirin in HCV patients. J. Clin. Gastroenterol. 2009, 43:661-671.
21. de Bruijne J., Weegink C.J., Jansen P.L., Reesink H.W. New developments in the antiviral treatment of hepatitis C. Vox Sang. 2009, 97:1-12.
22. Missale G., Bertoni R., Lamonaca V., Valli A., Massari M., Mori C., Rumi M.G., Houghton M., Fiaccadori F., Ferrari C. Different clinical behaviors of acute hepatitis C virus infection are associated with different vigor of the anti-viral cell-mediated immune response. J. Clin. Invest. 1996, 98:706-714.
23. Chang K.M., Thimme R., Melpolder J.J., Oldach D., Pemberton J., Moorhead-Loudis J., McHutchison J.G., Alter H.J., Chisari F.V. Differential CD4(+) and CD8(+) T-cell responsiveness in hepatitis C virus infection. Hepatology 2001, 33:267-276.
24. Thimme R., Oldach D., Chang K.M., Steiger C., Ray S.C., Chisari F.V. Determinants of viral clearance and persistence during acute hepatitis C virus infection. J. Exp. Med. 2001, 194:1395-1406.
25. Rehermann B. Interaction between the hepatitis C virus and the immune system. Semin. Liver Dis. 2000, 20:127-141.
26. Rehermann B. Chronic infections with hepatotropic viruses: mechanisms of impairment of cellular immune responses. Semin. Liver Dis. 2007, 27:152-160.
27. Rehermann B. Hepatitis C virus versus innate and adaptive immune responses: a tale of coevolution and coexistence. J. Clin. Invest. 2009, 119:1745-1754.
28. Boonstra A., Woltman A.M., Janssen H.L. Immunology of hepatitis B and hepatitis C virus infections. Best Pract. Res. Clin. Gastroenterol. 2008, 22:1049-1061.
29. Irshad M., Khushboo I., Singh S. Hepatitis C virus (HCV): a review of immunological aspects. Int. Rev. Immunol. 2008, 27:497-517.
30. Kanto T., Hayashi N. Immunopathogenesis of hepatitis C virus infection: multifaceted strategies subverting innate and adaptive immunity. Intern. Med. 2006, 45:183-191.
31. + T cells with viral clearance in acute hepatitis C. J. Infect. Dis. 2000, 181:1528-1536.
32. Lechner F., Sullivan J., Spiegel H., Nixon D.F., Ferrari B., Davis A., Borkowsky B., Pollack H., Barnes E., Dusheiko G., Klenerman P. Why do cytotoxic T lymphocytes fail to eliminate hepatitis C virus? Lessons from studies using major histocompatibility complex class I peptide tetramers. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2000, 355:1085-1092.
33. Pearlman B.L. Hepatitis C infection: a clinical review. South. Med. J. 2004, 97:364-373. quiz 374.
34. Salem M.L., Alenzi F.Q., Nath N., El-Naggar S.A., Al-Khami A.A., Al-Jabri A.A., Arif J., El-Nashar I.M., El-Tounsi I., Wyse R.N. Plasticity of T cell differentiation and cytokine signature: a double-edged sword for immune responses. Immunol. Endocr. Metab. Agents Med. Chem. (IEMAMC) 2009, 9:90-105.
35. Chang K.M. Regulatory T cells in hepatitis C virus infection. Hepatol. Res. 2007, 37(Suppl. 3):S327-S330.
36. Gabrilovich D.I., Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 2009, 9:162-174.
37. Nagaraj S., Gabrilovich D.I. Myeloid-derived suppressor cells. Adv. Exp. Med. Biol. 2007, 601:213-223.
38. Ilkovitch D., Lopez D.M. The liver is a site for tumor-induced myeloid-derived suppressor cell accumulation and immunosuppression. Cancer Res. 2009, 69:5514-5521.
39. Abe T., Kaname Y., Hamamoto I., Tsuda Y., Wen X., Taguwa S., Moriishi K., Takeuchi O., Kawai T., Kanto T., Hayashi N., Akira S., Matsuura Y. Hepatitis C virus nonstructural protein 5A modulates the toll-like receptor-MyD88-dependent signaling pathway in macrophage cell lines. J. Virol. 2007, 81:8953-8966.
40. Agaugue S., Perrin-Cocon L., Andre P., Lotteau V. Hepatitis C lipo-Viro-particle from chronically infected patients interferes with TLR4 signaling in dendritic cell. PLoS One 2007, 2:e330.
41. Chang S., Dolganiuc A., Szabo G. Toll-like receptors 1 and 6 are involved in TLR2-mediated macrophage activation by hepatitis C virus core and NS3 proteins. J. Leukoc. Biol. 2007, 82:479-487.
42. Mozer-Lisewska I., Sluzewski W., Kaczmarek M., Jenek R., Szczepanski M., Figlerowicz M., Kowala-Piaskowska A., Zeromski J. Tissue localization of Toll-like receptors in biopsy specimens of liver from children infected with hepatitis C virus. Scand. J. Immunol. 2005, 62:407-412.
43. Sato K., Ishikawa T., Okumura A., Yamauchi T., Sato S., Ayada M., Matsumoto E., Hotta N., Oohashi T., Fukuzawa Y., Kakumu S. Expression of Toll-like receptors in chronic hepatitis C virus infection. J. Gastroenterol. Hepatol. 2007, 22:1627-1632.
44. Stadlbauer V., Mookerjee R.P., Wright G.A., Davies N.A., Jurgens G., Hallstrom S., Jalan R. Role of Toll-like receptors 2, 4, and 9 in mediating neutrophil dysfunction in alcoholic hepatitis. Am. J. Physiol. Gastrointest. Liver Physiol. 2009, 296:G15-G22.
45. Hemmi H., Akira S. TLR signalling and the function of dendritic cells. Chem. Immunol. Allergy 2005, 86:120-135.
46. Blander J.M. Phagocytosis and antigen presentation: a partnership initiated by Toll-like receptors. Ann. Rheum. Dis. 2008, 67(Suppl. 3):iii44-iii49.
47. Broering R., Wu J., Meng Z., Hilgard P., Lu M., Trippler M., Szczeponek A., Gerken G., Schlaak J.F. Toll-like receptor-stimulated non-parenchymal liver cells can regulate hepatitis C virus replication. J. Hepatol. 2008, 48:914-922.
48. Chatila T.A. Regulatory T cells: key players in tolerance and autoimmunity. Endocrinol. Metab. Clin. North Am. 2009, 38:265-272. vi.
49. + T cells. Proc. Natl. Acad. Sci. USA 2002, 99:8832-8837.
50. Mills K.H. Regulatory T cells: friend or foe in immunity to infection?. Nat Rev Immunol 2004, 4:841-855.
51. Alatrakchi N., Koziel M. Regulatory T cells and viral liver disease. J. Viral Hepat. 2009, 16:223-229.
52. Barboza L., Salmen S., Goncalves L., Colmenares M., Peterson D., Montes H., Cartagirone R., Gutierrez Mdel C., Berrueta L. Antigen-induced regulatory T cells in HBV chronically infected patients. Virology 2007, 368:41-49.
53. Carpentier A., Conti F., Stenard F., Aoudjehane L., Miroux C., Podevin P., Morales O., Chouzenoux S., Scatton O., Groux H., Auriault C., Calmus Y., Pancre V., Delhem N. Increased expression of regulatory Tr1 cells in recurrent hepatitis C after liver transplantation. Am. J. Transplant 2009.
54. Diaz-Montero C.M., Salem M.L., Nishimura M.I., Garrett-Mayer E., Cole D.J., Montero A.J. Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin-cyclophosphamide chemotherapy. Cancer Immunol. Immunother. 2009, 58:49-59.
55. Dolcetti L., Marigo I., Mantelli B., Peranzoni E., Zanovello P., Bronte V. Myeloid-derived suppressor cell role in tumor-related inflammation. Cancer Lett. 2008, 267:216-225.
56. Almand B., Clark J.I., Nikitina E., van Beynen J., English N.R., Knight S.C., Carbone D.P., Gabrilovich D.I. Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer. J. Immunol. 2001, 166:678-689.
57. Mandruzzato S., Solito S., Falisi E., Francescato S., Chiarion-Sileni V., Mocellin S., Zanon A., Rossi C.R., Nitti D., Bronte V., Zanovello P. IL4Ralpha+ myeloid-derived suppressor cell expansion in cancer patients. J. Immunol. 2009, 182:6562-6568.
58. Haile L.A., von Wasielewski R., Gamrekelashvili J., Kruger C., Bachmann O., Westendorf A.M., Buer J., Liblau R., Manns M.P., Korangy F., Greten T.F. Myeloid-derived suppressor cells in inflammatory bowel disease: a new immunoregulatory pathway. Gastroenterology 2008, 135:871-881. 881 e1-5.
59. Hoechst B., Voigtlaender T., Ormandy L., Gamrekelashvili J., Zhao F., Wedemeyer H., Lehner F., Manns M.P., Greten T.F., Korangy F. Myeloid derived suppressor cells inhibit natural killer cells in patients with hepatocellular carcinoma via the NKp30 receptor. Hepatology 2009.
60. Hoechst B., Ormandy L.A., Ballmaier M., Lehner F., Kruger C., Manns M.P., Greten T.F., Korangy F. A new population of myeloid-derived suppressor cells in hepatocellular carcinoma patients induces CD4(+)CD25(+)Foxp3(+) T cells. Gastroenterology 2008, 135:234-243.
61. Oh U., Blevins G., Griffith C., Richert N., Maric D., Lee C.R., McFarland H., Jacobson S. Regulatory T cells are reduced during anti-CD25 antibody treatment of multiple sclerosis. Arch. Neurol. 2009, 66:471-479.
62. Wang Z., Xiao L., Shi B.Y., Qian Y.Y., Bai H.W., Chang J.Y., Cai M. Short-term anti-CD25 monoclonal antibody treatment and neogenetic CD4(+)CD25(high) regulatory T cells in kidney transplantation. Transpl. Immunol. 2008, 19:69-73.
63. Platz K.P., Braun F., Fandrich F., Kremer B., Mueller A.R. IL-2 antagonists: the European perspective. Transplant. Proc. 2005, 37:1783-1784.
64. Duvic M., Talpur R. Optimizing denileukin diftitox (Ontak) therapy. Future Oncol. 2008, 4:457-469.
65. Barnett B.G., Ruter J., Kryczek I., Brumlik M.J., Cheng P.J., Daniel B.J., Coukos G., Zou W., Curiel T.J. Regulatory T cells: a new frontier in cancer immunotherapy. Adv. Exp. Med. Biol. 2008, 622:255-260.
66. Xin H., Zhang C., Herrmann A., Du Y., Figlin R., Yu H. Sunitinib inhibition of Stat3 induces renal cell carcinoma tumor cell apoptosis and reduces immunosuppressive cells. Cancer Res. 2009, 69:2506-2513.
67. + regulatory T cells. Br. J. Haematol. 2009, 144:195-205.
68. Ozao-Choy J., Ma G., Kao J., Wang G.X., Meseck M., Sung M., Schwartz M., Divino C.M., Pan P.Y., Chen S.H. The novel role of tyrosine kinase inhibitor in the reversal of immune suppression and modulation of tumor microenvironment for immune-based cancer therapies. Cancer Res. 2009, 69:2514-2522.
69. Apolloni E., Bronte V., Mazzoni A., Serafini P., Cabrelle A., Segal D.M., Young H.A., Zanovello P. Immortalized myeloid suppressor cells trigger apoptosis in antigen-activated T lymphocytes. J. Immunol. 2000, 165:6723-6730.
70. + T lymphocytes after immunization: induction of a suppressive population of Mac-1+/Gr-1+ cells. J. Immunol. 1998, 161:5313-5320.
71. Yang L., DeBusk L.M., Fukuda K., Fingleton B., Green-Jarvis B., Shyr Y., Matrisian L.M., Carbone D.P., Lin P.C. Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell 2004, 6:409-421.
72. Ko J.S., Bukowski R.M., Fincke J.H. Myeloid-derived suppressor cells: a novel therapeutic target. Curr. Oncol. Rep. 2009, 11:87-93.
73. Ko J.S., Zea A.H., Rini B.I., Ireland J.L., Elson P., Cohen P., Golshayan A., Rayman P.A., Wood L., Garcia J., Dreicer R., Bukowski R., Finke J.H. Sunitinib mediates reversal of myeloid-derived suppressor cell accumulation in renal cell carcinoma patients. Clin. Cancer Res. 2009, 15:2148-2157.
74. Kusmartsev S., Su Z., Heiser A., Dannull J., Eruslanov E., Kubler H., Yancey D., Dahm P., Vieweg J. Reversal of myeloid cell-mediated immunosuppression in patients with metastatic renal cell carcinoma. Clin. Cancer Res. 2008, 14:8270-8278.
75. + regulatory T cells in tumor immune escape. Chin. J. Cancer 2009, 28:184-187.
76. Frumento G., Piazza T., Di Carlo E., Ferrini S. Targeting tumor-related immunosuppression for cancer immunotherapy. Endocr. Metab. Immune Disord. Drug Targets 2006, 6:233-237.
77. Boasso A., Vaccari M., Fuchs D., Hardy A.W., Tsai W.P., Tryniszewska E., Shearer G.M., Franchini G. Combined effect of antiretroviral therapy and blockade of IDO in SIV-infected rhesus macaques. J. Immunol. 2009, 182:4313-4320.
78. Lob S., Konigsrainer A., Schafer R., Rammensee H.G., Opelz G., Terness P. Levo- but not dextro-1-methyl tryptophan abrogates the IDO activity of human dendritic cells. Blood 2008, 111:2152-2154.
79. Qian F., Villella J., Wallace P.K., Mhawech-Fauceglia P., Tario J.D., Andrews C., Matsuzaki J., Valmori D., Ayyoub M., Frederick P.J., Beck A., Liao J., Cheney R., Moysich K., Lele S., Shrikant P., Old L.J., Odunsi K. Efficacy of levo-1-methyl tryptophan and dextro-1-methyl tryptophan in reversing indoleamine-2,3-dioxygenase-mediated arrest of T-cell proliferation in human epithelial ovarian cancer. Cancer Res. 2009, 69:5498-5504.
80. Cottalorda A., Verschelde C., Marcais A., Tomkowiak M., Musette P., Uematsu S., Akira S., Marvel J., Bonnefoy-Berard N. TLR2 engagement on CD8 T cells lowers the threshold for optimal antigen-induced T cell activation. Eur. J. Immunol. 2006, 36:1684-1693.
81. + T cells in chronic colitis. J. Immunol. 2008, 180:5291-5299.
82. + T cells and augments their antigen-specific responses upon their adoptive transfer into naive recipient mice. Vaccine 2009, 27:549-557.
83. Seya T., Akazawa T., Tsujita T., Matsumoto M. Role of Toll-like receptors in adjuvant-augmented immune therapies. Evid. Based Complement Altern. Med. 2006, 3:31-38. discussion 133-137.
84. Kawai T., Akira S. TLR signaling. Semin. Immunol. 2007, 19:24-32.
85. Kabelitz D. Expression and function of Toll-like receptors in T lymphocytes. Curr. Opin. Immunol. 2007, 19:39-45.
86. Dai J., Liu B., Li Z. Regulatory T cells and Toll-like receptors: what is the missing link?. Int. Immunopharmacol. 2009, 9:528-533.
87. Nyirenda M.H., O'Brien K., Sanvito L., Constantinescu C.S., Gran B. Modulation of regulatory T cells in health and disease: role of toll-like receptors. Inflamm. Allergy Drug Targets 2009, 8:124-129.
88. regs: to suppress or not to suppress?. Immunology 2008, 124:445-452.
89. + T cell. Int. Immunol. 2007, 19:193-201.
90. + T cells. Immunol. Lett. 2007, 108:183-188.
91. Sutmuller R.P., den Brok M.H., Kramer M., Bennink E.J., Toonen L.W., Kullberg B.J., Joosten L.A., Akira S., Netea M.G., Adema G.J. Toll-like receptor 2 controls expansion and function of regulatory T cells. J. Clin. Invest. 2006, 116:485-494.
92. + regulatory T cell function. Science 2005, 309:1380-1384.
93. Ko H.J., Lee J.M., Kim Y.J., Kim Y.S., Lee K.A., Kang C.Y. Immunosuppressive myeloid-derived suppressor cells can be converted into immunogenic APCs with the help of activated NKT cells: an alternative cell-based antitumor vaccine. J. Immunol. 2009, 182:1818-1828.
94. Salem M.L., Kadima A.N., Cole D.J., Gillanders W.E. Defining the antigen-specific T-cell response to vaccination and poly(I:C)/TLR3 signaling: evidence of enhanced primary and memory CD8 T-cell responses and antitumor immunity. J. Immunother. 2005, 28:220-228.
95. Salem M.L., Diaz-Montero C.M., Al-Khami A.A., El-Naggar S.A., Naga O., Montero A.J., Khafagy A., Cole D.J. Recovery from cyclophosphamide-induced lymphopenia results in expansion of immature dendritic cells which can mediate enhanced prime-boost vaccination antitumor responses in vivo when stimulated with the TLR3 agonist poly(I:C). J. Immunol. 2009, 182:2030-2040.
96. reg cells? A double-edged sword in immunity to tumours. Oncogene 2008, 27:168-180.
97. + T regulatory cells. J. Immunol. 2005, 175:8051-8059.
98. Okugawa S., Yanagimoto S., Tsukada K., Kitazawa T., Koike K., Kimura S., Nagase H., Hirai K., Ota Y. Bacterial flagellin inhibits T cell receptor-mediated activation of T cells by inducing suppressor of cytokine signalling-1 (SOCS-1). Cell. Microbiol. 2006, 8:1571-1580.
99. Uematsu S., Jang M.H., Chevrier N., Guo Z., Kumagai Y., Yamamoto M., Kato H., Sougawa N., Matsui H., Kuwata H., Hemmi H., Coban C., Kawai T., Ishii K.J., Takeuchi O., Miyasaka M., Takeda K., Akira S. Detection of pathogenic intestinal bacteria by Toll-like receptor 5 on intestinal CD11c(+) lamina propria cells. Nat. Immunol. 2006, 7:868-874.
100. Szabo G., Dolganiuc A. Hepatitis C and innate immunity: recent advances. Clin. Liver Dis. 2008, 12:675-692. x.
101. Steinman R.M., Hemmi H. Dendritic cells: translating innate to adaptive immunity. Curr. Top. Microbiol. Immunol. 2006, 311:17-58.
102. Banchereau J., Fay J., Pascual V., Palucka A.K. Dendritic cells: controllers of the immune system and a new promise for immunotherapy. Novartis Found. Symp. 2003, 252:226-235. discussion 235-238, 257-267.
103. + T cells. Nat. Immunol. 2001, 2:1010-1017.
104. Banchereau J., Palucka A.K. Dendritic cells as therapeutic vaccines against cancer. Nat. Rev. Immunol. 2005, 5:296-306.
105. Mellor J., Haydon G., Blair C., Livingstone W., Simmonds P. Low level or absent in vivo replication of hepatitis C virus and hepatitis G virus/GB virus C in peripheral blood mononuclear cells. J. Gen. Virol. 1998, 79(Pt. 4):705-714.
106. Pachiadakis I., Pollara G., Chain B.M., Naoumov N.V. Is hepatitis C virus infection of dendritic cells a mechanism facilitating viral persistence?. Lancet Infect. Dis. 2005, 5:296-304.
107. Akbar S.M., Horiike N., Onji M., Hino O. Dendritic cells and chronic hepatitis virus carriers. Intervirology 2001, 44:199-208.
108. Kanto T. Virus associated innate immunity in liver. Front. Biosci. 2008, 13:6183-6192.
109. Kanto T., Hayashi N. Innate immunity in hepatitis C virus infection: interplay among dendritic cells, natural killer cells and natural killer T cells. Hepatol. Res. 2007, 37(Suppl. 3):S319-S326.
110. Xu N., Yao H.P., Sun Z., Chen Z. Toll-like receptor 7 and 9 expression in peripheral blood mononuclear cells from patients with chronic hepatitis B and related hepatocellular carcinoma. Acta Pharmacol. Sin. 2008, 29:239-244.
111. Yakushijin T., Kanto T., Inoue M., Oze T., Miyazaki M., Itose I., Miyatake H., Sakakibara M., Kuzushita N., Hiramatsu N., Takehara T., Kasahara A., Hayashi N. Reduced expression and functional impairment of Toll-like receptor 2 on dendritic cells in chronic hepatitis C virus infection. Hepatol. Res. 2006, 34:156-162.
112. Breiman A., Grandvaux N., Lin R., Ottone C., Akira S., Yoneyama M., Fujita T., Hiscott J., Meurs E.F. Inhibition of RIG-I-dependent signaling to the interferon pathway during hepatitis C virus expression and restoration of signaling by IKKepsilon. J. Virol. 2005, 79:3969-3978.
113. Chen Z., Cheng Y., Xu Y., Liao J., Zhang X., Hu Y., Zhang Q., Wang J., Zhang Z., Shen F., Yuan Z. Expression profiles and function of Toll-like receptors 2 and 4 in peripheral blood mononuclear cells of chronic hepatitis B patients. Clin. Immunol. 2008, 128:400-408.
114. Dolganiuc A., Chang S., Kodys K., Mandrekar P., Bakis G., Cormier M., Szabo G. Hepatitis C virus (HCV) core protein-induced, monocyte-mediated mechanisms of reduced IFN-alpha and plasmacytoid dendritic cell loss in chronic HCV infection. J. Immunol. 2006, 177:6758-6768.
115. Eid A.J., Brown R.A., Paya C.V., Razonable R.R. Association between toll-like receptor polymorphisms and the outcome of liver transplantation for chronic hepatitis C virus. Transplantation 2007, 84:511-516.
116. He Q., Graham C.S., Durante Mangoni E., Koziel M.J. Differential expression of toll-like receptor mRNA in treatment non-responders and sustained virologic responders at baseline in patients with chronic hepatitis C. Liver Int. 2006, 26:1100-1110.
117. Villacres M.C., Literat O., DeGiacomo M., Du W., Frederick T., Kovacs A. Defective response to Toll-like receptor 3 and 4 ligands by activated monocytes in chronic hepatitis C virus infection. J. Viral Hepat. 2008, 15:137-144.
118. Wu J., Meng Z., Jiang M., Pei R., Trippler M., Broering R., Bucchi A., Sowa J.P., Dittmer U., Yang D., Roggendorf M., Gerken G., Lu M., Schlaak J.F. Hepatitis B virus suppresses toll-like receptor-mediated innate immune responses in murine parenchymal and nonparenchymal liver cells. Hepatology 2009, 49:1132-1140.
119. Xie Q., Shen H.C., Jia N.N., Wang H., Lin L.Y., An B.Y., Gui H.L., Guo S.M., Cai W., Yu H., Guo Q., Bao S. Patients with chronic hepatitis B infection display deficiency of plasmacytoid dendritic cells with reduced expression of TLR9. Microbes Infect. 2009, 11:515-523.
120. Zhou J., Huang Y., Tian D., Xu D., Chen M., Wu H. Expression of toll-like receptor 9 in peripheral blood mononuclear cells from patients with different hepatitis B and C viral loads. J. Huazhong Univ. Sci. Technolog. Med. Sci. 2009, 29:313-317.
121. Takehara T., Hayashi N. Natural killer cells in hepatitis C virus infection: from innate immunity to adaptive immunity. Clin. Gastroenterol. Hepatol. 2005, 3:S78-S81.
122. Golden-Mason L., Rosen H.R. Natural killer cells: primary target for hepatitis C virus immune evasion strategies?. Liver Transpl. 2006, 12:363-372.
123. Yao Z.Q., King E., Prayther D., Yin D., Moorman J. T cell dysfunction by hepatitis C virus core protein involves PD-1/PDL-1 signaling. Viral. Immunol. 2007, 20:276-287.
124. Urbani S., Amadei B., Tola D., Pedrazzi G., Sacchelli L., Cavallo M.C., Orlandini A., Missale G., Ferrari C. Restoration of HCV-specific T cell functions by PD-1/PD-L1 blockade in HCV infection: effect of viremia levels and antiviral treatment. J. Hepatol. 2008, 48:548-558.
125. + T cell responses in a hepatitis C virus core murine model. J. Immunol. 2008, 180:4875-4884.
126. Golden-Mason L., Klarquist J., Wahed A.S., Rosen H.R. Cutting edge: programmed death-1 expression is increased on immunocytes in chronic hepatitis C virus and predicts failure of response to antiviral therapy: race-dependent differences. J. Immunol. 2008, 180:3637-3641.
127. + T cells during acute HCV infection, irrespective of clinical outcome. J. Virol. 2008, 82:3154-3160.
128. Ebihara T., Shingai M., Matsumoto M., Wakita T., Seya T. Hepatitis C virus-infected hepatocytes extrinsically modulate dendritic cell maturation to activate T cells and natural killer cells. Hepatology 2008, 48:48-58.
129. Jinushi M., Takehara T., Tatsumi T., Kanto T., Miyagi T., Suzuki T., Kanazawa Y., Hiramatsu N., Hayashi N. Negative regulation of NK cell activities by inhibitory receptor CD94/NKG2A leads to altered NK cell-induced modulation of dendritic cell functions in chronic hepatitis C virus infection. J. Immunol. 2004, 173:6072-6081.
130. Jinushi M., Takehara T., Kanto T., Tatsumi T., Groh V., Spies T., Miyagi T., Suzuki T., Sasaki Y., Hayashi N. Critical role of MHC class I-related chain A and B expression on IFN-alpha-stimulated dendritic cells in NK cell activation: impairment in chronic hepatitis C virus infection. J. Immunol. 2003, 170:1249-1256.
131. Fajardo-Moser M., Berzel S., Moll H. Mechanisms of dendritic cell-based vaccination against infection. Int. J. Med. Microbiol. 2008, 298:11-20.
132. + T cell responses are partially dependent on NK cells with the induction of a beneficial cytokine milieu. Vaccine 2006, 24:5119-5132.
133. Lore K., Betts M.R., Brenchley J.M., Kuruppu J., Khojasteh S., Perfetto S., Roederer M., Seder R.A., Koup R.A. Toll-like receptor ligands modulate dendritic cells to augment cytomegalovirus- and HIV-1-specific T cell responses. J. Immunol. 2003, 171:4320-4328.
134. Edwards A.D., Diebold S.S., Slack E.M., Tomizawa H., Hemmi H., Kaisho T., Akira S., Reis e Sousa C. Toll-like receptor expression in murine DC subsets: lack of TLR7 expression by CD8 alpha+ DC correlates with unresponsiveness to imidazoquinolines. Eur. J. Immunol. 2003, 33:827-833.
135. Datta S.K., Redecke V., Prilliman K.R., Takabayashi K., Corr M., Tallant T., DiDonato J., Dziarski R., Akira S., Schoenberger S.P., Raz E. A subset of Toll-like receptor ligands induces cross-presentation by bone marrow-derived dendritic cells. J. Immunol. 2003, 170:4102-4110.
136. Kadowaki N., Ho S., Antonenko S., Malefyt R.W., Kastelein R.A., Bazan F., Liu Y.J. Subsets of human dendritic cell precursors express different toll-like receptors and respond to different microbial antigens. J. Exp. Med. 2001, 194:863-869.
137. West M.A., Wallin R.P., Matthews S.P., Svensson H.G., Zaru R., Ljunggren H.G., Prescott A.R., Watts C. Enhanced dendritic cell antigen capture via toll-like receptor-induced actin remodeling. Science 2004, 305:1153-1157.
138. Meyer T., Stockfleth E. Clinical investigations of Toll-like receptor agonists. Expert Opin. Investig. Drugs 2008, 17:1051-1065.
139. Tirapu I., Giquel B., Alexopoulou L., Uematsu S., Flavell R., Akira S., Diebold S.S. PolyI:C-induced reduction in uptake of soluble antigen is independent of dendritic cell activation. Int. Immunol. 2009, 21:871-879.
140. Jasani B., Navabi H., Adams M. Ampligen: a potential toll-like 3 receptor adjuvant for immunotherapy of cancer. Vaccine 2009, 27:3401-3404.
141. Boullart A.C., Aarntzen E.H., Verdijk P., Jacobs J.F., Schuurhuis D.H., Benitez-Ribas D., Schreibelt G., van de Rakt M.W., Scharenborg N.M., de Boer A., Kramer M., Figdor C.G., Punt C.J., Adema G.J., de Vries I.J. Maturation of monocyte-derived dendritic cells with Toll-like receptor 3 and 7/8 ligands combined with prostaglandin E2 results in high interleukin-12 production and cell migration. Cancer Immunol. Immunother. 2008, 57:1589-1597.
142. Renn C.N., Sanchez D.J., Ochoa M.T., Legaspi A.J., Oh C.K., Liu P.T., Krutzik S.R., Sieling P.A., Cheng G., Modlin R.L. TLR activation of langerhans cell-like dendritic cells triggers an antiviral immune response. J. Immunol. 2006, 177:298-305.
143. Walker J., Tough D.F. Modification of TLR-induced activation of human dendritic cells by type I IFN: synergistic interaction with TLR4 but not TLR3 agonists. Eur. J. Immunol. 2006.
144. Navabi H., Jasani B., Reece A., Clayton A., Tabi Z., Donninger C., Mason M., Adams M. A clinical grade poly I:C-analogue (Ampligen) promotes optimal DC maturation and Th1-type T cell responses of healthy donors and cancer patients in vitro. Vaccine 2009, 27:107-115.
145. Adams M., Navabi H., Jasani B., Man S., Fiander A., Evans A.S., Donninger C., Mason M. Dendritic cell (DC) based therapy for cervical cancer: use of DC pulsed with tumour lysate and matured with a novel synthetic clinically non-toxic double stranded RNA analogue poly [I]:poly [C(12)U] (Ampligen R). Vaccine 2003, 21:787-790.
146. Mailliard R.B., Wankowicz-Kalinska A., Cai Q., Wesa A., Hilkens C.M., Kapsenberg M.L., Kirkwood J.M., Storkus W.J., Kalinski P. Alpha-type-1 polarized dendritic cells: a novel immunization tool with optimized CTL-inducing activity. Cancer Res. 2004, 64:5934-5937.
147. Wang R.F., Miyahara Y., Wang H.Y. Toll-like receptors and immune regulation: implications for cancer therapy. Oncogene 2008, 27:181-189.
148. Paulos C.M., Kaiser A., Wrzesinski C., Hinrichs C.S., Cassard L., Boni A., Muranski P., Sanchez-Perez L., Palmer D.C., Yu Z., Antony P.A., Gattinoni L., Rosenberg S.A., Restifo N.P. Toll-like receptors in tumor immunotherapy. Clin. Cancer Res. 2007, 13:5280-5289.
149. Xia C., Lu M., Zhang Z., Meng Z., Shi C. TLRs antiviral effect on hepatitis B virus in HepG2 cells. J. Appl. Microbiol. 2008, 105:1720-1727.
150. Guo H., Jiang D., Ma D., Chang J., Dougherty A.M., Cuconati A., Block T.M., Guo J.T. Activation of pattern recognition receptor-mediated innate immunity inhibits the replication of hepatitis B virus in human hepatocyte-derived cells. J. Virol. 2009, 83:847-858.
151. Lee J., Wu C.C., Lee K.J., Chuang T.H., Katakura K., Liu Y.T., Chan M., Tawatao R., Chung M., Shen C., Cottam H.B., Lai M.M., Raz E., Carson D.A. Activation of anti-hepatitis C virus responses via Toll-like receptor 7. Proc. Natl. Acad. Sci. USA 2006, 103:1828-1833.
152. Zhang X., Meng Z., Qiu S., Xu Y., Yang D., Schlaak J.F., Roggendorf M., Lu M. Lipopolysaccharide induced innate immune responses in primary hepatocytes down-regulates woodchuck hepatitis virus replication via interferon-independent pathways. Cell Microbiol. 2009.
153. Horsmans Y., Berg T., Desager J.P., Mueller T., Schott E., Fletcher S.P., Steffy K.R., Bauman L.A., Kerr B.M., Averett D.R. Isatoribine, an agonist of TLR7, reduces plasma virus concentration in chronic hepatitis C infection. Hepatology 2005, 42:724-731.
154. Schott E., Witt H., Neumann K., Bergk A., Halangk J., Weich V., Muller T., Puhl G., Wiedenmann B., Berg T. Association of TLR7 single nucleotide polymorphisms with chronic HCV-infection and response to interferon-a-based therapy. J. Viral Hepat. 2008, 15:71-78.
155. Fletcher S., Steffy K., Averett D. Masked oral prodrugs of toll-like receptor 7 agonists: a new approach for the treatment of infectious disease. Curr. Opin. Investig. Drugs 2006, 7:702-708.
156. Xiang A.X., Webber S.E., Kerr B.M., Rueden E.J., Lennox J.R., Haley G.J., Wang T., Ng J.S., Herbert M.R., Clark D.L., Banh V.N., Li W., Fletcher S.P., Steffy K.R., Bartkowski D.M., Kirkovsky L.I., Bauman L.A., Averett D.R. Discovery of ANA975: an oral prodrug of the TLR-7 agonist isatoribine. Nucleosides Nucleotides Nucleic Acids 2007, 26:635-640.
157. Roberts S.K., Cooksley G., Dore G.J., Robson R., Shaw D., Berns H., Hill G., Klumpp K., Najera I., Washington C. Robust antiviral activity of R1626, a novel nucleoside analog: a randomized, placebo-controlled study in patients with chronic hepatitis C. Hepatology 2008, 48:398-406.
158. McHutchison J.G., Bacon B.R., Gordon S.C., Lawitz E., Shiffman M., Afdhal N.H., Jacobson I.M., Muir A., Al-Adhami M., Morris M.L., Lekstrom-Himes J.A., Efler S.M., Davis H.L. Phase 1B, randomized, double-blind, dose-escalation trial of CPG 10101 in patients with chronic hepatitis C virus. Hepatology 2007, 46:1341-1349.
159. Butowski N., Chang S.M., Junck L., Deangelis L.M., Abrey L., Fink K., Cloughesy T., Lamborn K.R., Salazar A.M., Prados M.D. A phase II clinical trial of poly-ICLC with radiation for adult patients with newly diagnosed supratentorial glioblastoma: a North American Brain Tumor Consortium (NABTC01-05). J. Neurooncol. 2009, 91:175-182.
160. Butowski N., Lamborn K.R., Lee B.L., Prados M.D., Cloughesy T., Deangelis L.M., Abrey L., Fink K., Lieberman F., Mehta M., Ian Robins H., Junck L., Salazar A.M., Chang S.M. A North American brain tumor consortium phase II study of poly-ICLC for adult patients with recurrent anaplastic gliomas. J. Neurooncol. 2009, 91:183-189.
161. Ewel C.H., Urba W.J., Kopp W.C., Smith J.W., Steis R.G., Rossio J.L., Longo D.L., Jones M.J., Alvord W.G., Pinsky C.M., et al. Polyinosinic-polycytidylic acid complexed with poly-l-lysine and carboxymethylcellulose in combination with interleukin 2 in patients with cancer: clinical and immunological effects. Cancer Res. 1992, 52:3005-3010.
162. Salazar A.M., Levy H.B., Ondra S., Kende M., Scherokman B., Brown D., Mena H., Martin N., Schwab K., Donovan D., Dougherty D., Pulliam M., Ippolito M., Graves M., Brown H., Ommaya A. Long-term treatment of malignant gliomas with intramuscularly administered polyinosinic-polycytidylic acid stabilized with polylysine and carboxymethylcellulose: an open pilot study. Neurosurgery 1996, 38:1096-1103. discussion 1103-1104.
163. Zhu X., Nishimura F., Sasaki K., Fujita M., Dusak J.E., Eguchi J., Fellows-Mayle W., Storkus W.J., Walker P.R., Salazar A.M., Okada H. Toll like receptor-3 ligand poly-ICLC promotes the efficacy of peripheral vaccinations with tumor antigen-derived peptide epitopes in murine CNS tumor models. J. Transl. Med. 2007, 5:10.
164. Ichinohe T., Kawaguchi A., Tamura S., Takahashi H., Sawa H., Ninomiya A., Imai M., Itamura S., Odagiri T., Tashiro M., Chiba J., Sata T., Kurata T., Hasegawa H. Intranasal immunization with H5N1 vaccine plus Poly I:Poly C12U, a Toll-like receptor agonist, protects mice against homologous and heterologous virus challenge. Microbes Infect. 2007, 9:1333-1340.
165. Mismatched double-stranded RNA: polyI:polyC12U, Drugs R D 5 (2004) 297-304.
166. Bever C.T., McFarlin D.E., Levy H.B. A comparison of interferon responses to poly ICLC in males and females. J. Interferon Res. Spec. No. 1992, 85-90.
167. Megyeri K., Au W.C., Rosztoczy I., Raj N.B., Miller R.L., Tomai M.A., Pitha P.M. Stimulation of interferon and cytokine gene expression by imiquimod and stimulation by Sendai virus utilize similar signal transduction pathways. Mol. Cell. Biol. 1995, 15:2207-2218.
168. Koyama T., Sakamoto N., Tanabe Y., Nakagawa M., Itsui Y., Takeda Y., Kakinuma S., Sekine Y., Maekawa S., Yanai Y., Kurimoto M., Watanabe M. Divergent activities of interferon-alpha subtypes against intracellular hepatitis C virus replication. Hepatol. Res. 2006, 34:41-49.
169. Yamamoto S., Yano H., Sanou O., Ikegami H., Kurimoto M., Kojiro M. Different antiviral activities of IFN-alpha subtypes in human liver cell lines: synergism between IFN-alpha2 and IFN-alpha8. Hepatol. Res. 2002, 24:99.