Sustained hyperresponsiveness of dendritic cells is associated with spontaneous resolution of acute hepatitis C

Journal of Virology

Volumn 87, Issue 12, 2013, Pages 6769-6781

  Pelletier, Sandy ^a,b   Bédard, Nathalie ^a   Said, Elias ^a,b,c   Ancuta, Petronela ^a,b   Bruneau, Julie ^a,b   Shoukry, Naglaa H ^a,b  

^a UNIVERSITY OF MONTREAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c SULTAN QABOOS UNIVERSITY   (Oman)

Author keywords

[No Author keywords available]

Indexed keywords

CD86 ANTIGEN; LIPOPOLYSACCHARIDE; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 LIGAND 2; SINGLE STRANDED RNA; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8;

ACUTE DISEASE; ADULT; ARTICLE; CELL FUNCTION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; FEMALE; HEPATITIS C; HIGH RISK PATIENT; HUMAN; INFECTION RISK; INTRAVENOUS DRUG ABUSE; MALE; MYELOID DENDRITIC CELL; PHENOTYPE; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RISK ASSESSMENT; VIRUS LOAD; VIRUS VIRULENCE;

ACUTE DISEASE; CELL DIFFERENTIATION; CYTOKINES; DENDRITIC CELLS; FEMALE; HEPACIVIRUS; HEPATITIS C; HEPATITIS C, CHRONIC; HUMANS; INTERLEUKINS; LIPOPOLYSACCHARIDES; MALE; SUBSTANCE ABUSE, INTRAVENOUS; T-LYMPHOCYTES; TOLL-LIKE RECEPTOR 4;

HEPATITIS C VIRUS;

EID: 84878540475     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02445-12     Document Type: Article

References (56)

1. Hoofnagle JH. 2002. Course and outcome of hepatitis C. Hepatology 36:S21-S29.
2. Rehermann B. 2009. Hepatitis C virus versus innate and adaptive immune responses: a tale of coevolution and coexistence. J. Clin. Invest. 119:1745-1754.
3. + T cell responses during longitudinal study of acute human hepatitis C. Hepatology 42:104-112.
4. Cox AL, Mosbruger T, Mao Q, Liu Z, Wang XH, Yang HC, Sidney J, Sette A, Pardoll D, Thomas DL, Ray SC. 2005. Cellular immune selection with hepatitis C virus persistence in humans. J. Exp. Med. 201:1741-1752.
5. Tester I, Smyk-Pearson S, Wang P, Wertheimer A, Yao E, Lewinsohn DM, Tavis JE, Rosen HR. 2005. Immune evasion versus recovery after acute hepatitis C virus infection from a shared source. J. Exp. Med. 201: 1725-1731.
6. Timm J, Lauer GM, Kavanagh DG, Sheridan I, Kim AY, Lucas M, Pillay T, Ouchi K, Reyor LL, Schulze Zur Wiesch J, Gandhi RT, Chung RT, Bhardwaj N, Klenerman P, Walker BD, Allen TM. 2004. CD8 epitope escape and reversion in acuteHCVinfection. J. Exp. Med. 200:1593-1604.
7. Grakoui A, Shoukry NH, Woollard DJ, Han JH, Hanson HL, Ghrayeb J, Murthy KK, Rice CM, Walker CM. 2003. HCV persistence and immune evasion in the absence of memory T cell help. Science 302:659-662.
8. Nakamoto N, Cho H, Shaked A, Olthoff K, Valiga ME, Kaminski M, Gostick E, Price DA, Freeman GJ, Wherry EJ, Chang KM. 2009. Synergistic reversal of intrahepatic HCV-specific CD8 T cell exhaustion by combined PD-1/CTLA-4 blockade. PLoS Pathog. 5:e1000313. doi:10 .1371/journal.ppat.1000313.
9. Penna A, Pilli M, Zerbini A, Orlandini A, Mezzadri S, Sacchelli L, Missale G, Ferrari C. 2007. Dysfunction and functional restoration of HCV-specific CD8 responses in chronic hepatitis C virus infection. Hepatology 45:588-601.
10. Radziewicz H, Ibegbu CC, Fernandez ML, Workowski KA, Obideen K, Wehbi M, Hanson HL, Steinberg JP, Masopust D, Wherry EJ, Altman JD, Rouse BT, Freeman GJ, Ahmed R, Grakoui A. 2007. Liverinfiltrating lymphocytes in chronic human hepatitis C virus infection display an exhausted phenotype with high levels of PD-1 and low levels of CD127 expression. J. Virol. 81:2545-2553.
11. + T cells undergo massive apoptosis in the peripheral blood during acuteHCVinfection and in the liver during the chronic phase of infection. J. Virol. 82:9808-9822.
12. + T-cell failure during chronic hepatitis C virus infection. Hepatology 42:828-837.
13. + T cells in chronic hepatitis C virus infection. J. Immunol. 169:3447-3458.
14. Joffre O, Nolte MA, Sporri R, Reis e Sousa C. 2009. Inflammatory signals in dendritic cell activation and the induction of adaptive immunity. Immunol. Rev. 227:234-247.
15. Kaiko GE, Horvat JC, Beagley KW, Hansbro PM. 2008. Immunological decision-making: how does the immune system decide to mount a helper T-cell response? Immunology 123:326-338.
16. Longman RS, Talal AH, Jacobson IM, Albert ML, Rice CM. 2004. Presence of functional dendritic cells in patients chronically infected with hepatitis C virus. Blood 103:1026-1029.
17. Ulsenheimer A, Gerlach JT, Jung MC, Gruener N, Wächtler M, Backmund M, Santantonio T, Schraut W, Heeg MH, Schirren CA, Zachoval R, Pape GR, Diepolder HM. 2005. Plasmacytoid dendritic cells in acute and chronic hepatitis C virus infection. Hepatology 41:643-651.
18. Goutagny N, Vieux C, Decullier E, Ligeoix B, Epstein A, Trepo C, Couzigou P, Inchauspe G, Bain C. 2004. Quantification and functional analysis of plasmacytoid dendritic cells in patients with chronic hepatitisC virus infection. J. Infect. Dis. 189:1646-1655.
19. Murakami H, Akbar SM, Matsui H, Horiike N, Onji M. 2004. Decreased interferon-alpha production and impaired T helper 1 polarization by dendritic cells from patients with chronic hepatitis C. Clin. Exp. Immunol. 137:559-565.
20. Della Bella S, Crosignani A, Riva A, Presicce P, Benetti A, Longhi R, Podda M, Villa ML. 2007. Decrease and dysfunction of dendritic cells correlate with impaired hepatitis C virus-specific CD4 T-cell proliferation in patients with hepatitis C virus infection. Immunology 121:283-292.
21. Kanto T, Inoue M, Miyatake H, Sato A, Sakakibara M, Yakushijin T, Oki C, Itose I, Hiramatsu N, Takehara T, Kasahara A, Hayashi N. 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.
22. Kanto T, Inoue M, Miyazaki M, Itose I, Miyatake H, Sakakibara M, Yakushijin T, Kaimori A, Oki C, Hiramatsu N, Kasahara A, Hayashi N. 2006. Impaired function of dendritic cells circulating in patients infected with hepatitis C virus who have persistently normal alanine aminotransferase levels. Intervirology 49:58-63.
23. Longman RS, Talal AH, Jacobson IM, Rice CM, Albert ML. 2005. Normal functional capacity in circulating myeloid and plasmacytoid dendritic cells in patients with chronic hepatitis C. J. Infect. Dis. 192:497-503.
24. Averill L, Lee WM, Karandikar NJ. 2007. Differential dysfunction in dendritic cell subsets during chronic HCV infection. Clin. Immunol. 123: 40-49.
25. Piccioli D, Tavarini S, Nuti S, Colombatto P, Brunetto M, Bonino F, Ciccorossi P, Zorat F, Pozzato G, Comar C, Abrignani S, Wack A. 2005. Comparable functions of plasmacytoid and monocyte-derived dendritic cells in chronic hepatitis C patients and healthy donors. J. Hepatol. 42:61-67.
26. + memory T cells. J. Virol. 82:10017-10031.
27. Roederer M, Nozzi JL, Nason MC. 2011. SPICE: exploration and analysis of post-cytometric complex multivariate datasets. Cytometry A 79:167- 174.
28. Wang JC, Kobie JJ, Zhang L, Cochran M, Mosmann TR, Ritchlin CT, Quataert SA. 2009. An 11-color flow cytometric assay for identifying, phenotyping, and assessing endocytic ability of peripheral blood dendritic cell subsets in a single platform. J. Immunol. Methods 341:106-116.
29. Pelletier S, Drouin C, Bedard N, Khakoo SI, Bruneau J, Shoukry NH. 2010. Increased degranulation of natural killer cells during acute HCV correlates with the magnitude of virus-specific T cell responses. J. Hepatol. 53:805- 816.
30. Gelinas JF, Fabre T, Willems P, Leung RC, George J, Willems B, Bruneau J, Shoukry NH. 3 March 2013. IL28B SNP screening and distribution in the French Canadian population using a rapid PCR-based test. Immunogenetics [Epub ahead of print.]. doi:10.1007/s00251-013-0688-7.
31. Rodrigue-Gervais IG, Jouan L, Beaule G, Sauve D, Bruneau J, Willems B, Sekaly RP, Lamarre D. 2007. Poly(I:C) and lipopolysaccharide innate sensing functions of circulating human myeloid dendritic cells are affected in vivo in hepatitis C virus-infected patients. J. Virol. 81:5537-5546.
32. Ida JA, Shrestha N, Desai S, Pahwa S, Hanekom WA, Haslett PA. 2006. A whole blood assay to assess peripheral blood dendritic cell function in response to Toll-like receptor stimulation. J. Immunol. Methods 310:86-99.
33. Werner JM, Heller T, Gordon AM, Sheets A, Sherker AH, Kessler E, Bean KS, Stevens M, Schmitt J, Rehermann B. 5 March 2013. Innate immune responses in hepatitisCvirus exposed healthcare workers who do not develop acute infection. Hepatology [Epub ahead of print.] doi:10 .1002/hep.26353.
34. Wertheimer AM, Bakke A, Rosen HR. 2004. Direct enumeration and functional assessment of circulating dendritic cells in patients with liver disease. Hepatology 40:335-345.
35. + lymphocytes in portal infiltrates in chronic hepatitis C. Histopathology 39:373-381.
36. Tanimoto K, Akbar SM, Michitaka K, Horiike N, Onji M. 2001. Antigen- presenting cells at the liver tissue in patients with chronic viral liver diseases: CD83-positive mature dendritic cells at the vicinity of focal and confluent necrosis. Hepatol. Res. 21:117-125.
37. Takahashi K, Asabe S, Wieland S, Garaigorta U, Gastaminza P, Isogawa M, Chisari FV. 2010. Plasmacytoid dendritic cells sense hepatitis C virusinfected cells, produce interferon, and inhibit infection. Proc. Natl. Acad. Sci. U. S. A. 107:7431-7436.
38. Swiecki M, Wang Y, Vermi W, Gilfillan S, Schreiber RD, Colonna M. 2011. Type I interferon negatively controls plasmacytoid dendritic cell numbers in vivo. J. Exp. Med. 208:2367-2374.
39. Sarasin-Filipowicz M, Oakeley EJ, Duong FH, Christen V, Terracciano L, Filipowicz W, Heim MH. 2008. Interferon signaling and treatment outcome in chronic hepatitis C. Proc. Natl. Acad. Sci. U. S. A. 105:7034-7039.
40. Stiffler JD, Nguyen M, Sohn JA, Liu C, Kaplan D, Seeger C. 2009. Focal distribution of hepatitis C virus RNA in infected livers. PLoS One 4:e6661. doi:10.1371/journal.pone.0006661.
41. Bigger CB, Brasky KM, Lanford RE. 2001. DNA microarray analysis of chimpanzee liver during acute resolving hepatitis C virus infection. J. Virol. 75:7059-7066.
42. Bigger CB, Guerra B, Brasky KM, Hubbard G, Beard MR, Luxon BA, Lemon SM, Lanford RE. 2004. Intrahepatic gene expression during chronic hepatitis C virus infection in chimpanzees. J. Virol. 78:13779-13792.
43. Su AI, Pezacki JP, Wodicka L, Brideau AD, Supekova L, Thimme R, Wieland S, Bukh J, Purcell RH, Schultz PG, Chisari FV. 2002. Genomic analysis of the host response to hepatitis C virus infection. Proc. Natl. Acad. Sci. U. S. A. 99:15669-15674.
44. Thimme R, Bukh J, Spangenberg HC, Wieland S, Pemberton J, Steiger C, Govindarajan S, Purcell RH, Chisari FV. 2002. Viral and immunological determinants of hepatitis C virus clearance, persistence, and disease. Proc. Natl. Acad. Sci. U. S. A. 99:15661-15668.
45. Chang KM. 2007. Regulatory T cells in hepatitis C virus infection. Hepatol. Res. 37(Suppl 3):S327-S330.
46. Manigold T, Racanelli V. 2007. T-cell regulation by CD4 regulatory T cells during hepatitis B and C virus infections: facts and controversies. Lancet Infect. Dis. 7:804-813.
47. + T cell polyfunctionality during chronic hepatitis C virus infection. J. Immunol. 184:3134-3144.
48. Dolganiuc A, Oak S, Kodys K, Golenbock DT, Finberg RW, Kurt-Jones E, Szabo G. 2004. Hepatitis C core and nonstructural 3 proteins trigger Toll-like receptor 2-mediated pathways and inflammatory activation. Gastroenterology 127:1513-1524.
49. Duesberg U, von dem Bussche A, Kirschning C, Miyake K, Sauerbruch T, Spengler U. 2002. Cell activation by synthetic lipopeptides of the hepatitisCvirus (HCV)-core protein is mediated by Toll like receptors (TLRs) 2 and 4. Immunol. Lett. 84:89-95.
50. Chung H, Watanabe T, Kudo M, Chiba T. 2010. Hepatitis C virus core protein induces homotolerance and cross-tolerance to Toll-like receptor ligands by activation of Toll-like receptor 2. J. Infect. Dis. 202:853-861.
51. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, Rao S, Kazzaz Z, Bornstein E, Lambotte O, Altmann D, Blazar BR, Rodriguez B, Teixeira-Johnson L, Landay A, Martin JN, Hecht FM, Picker LJ, Lederman MM, Deeks SG, Douek DC. 2006. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat. Med. 12:1365-1371.
52. Sandler NG, Koh C, Roque A, Eccleston JL, Siegel RB, Demino M, Kleiner DE, Deeks SG, Liang TJ, Heller T, Douek DC. 2011. Host response to translocated microbial products predicts outcomes of patients with HBV or HCV infection. Gastroenterology 141:1220-1230.
53. Dolganiuc A, Szabo G. 2011. Dendritic cells in hepatitis C infection: can they (help) win the battle? J. Gastroenterol. 46:432- 447.
54. Horner SM, Gale M, Jr. 2009. Intracellular innate immune cascades and interferon defenses that control hepatitis C virus. J. Interferon Cytokine Res. 29:489-498.
55. Li K, Lemon SM. 2013. Innate immune responses in hepatitis C virus infection. Semin. Immunopathol. 35:53-72.
56. Larsson M, Babcock E, Grakoui A, Shoukry N, Lauer G, Rice C, Walker C, Bhardwaj N. 2004. Lack of phenotypic and functional impairment in dendritic cells from chimpanzees chronically infected with hepatitis C virus. J. Virol. 78:6151-6161.