Innate immunity and hepatitis C virus infection: a microarray’s view

Infectious Agents and Cancer

Franco M Buonaguro¹  Maria Lina Tornesello¹  Annacarmen Petrizzo¹  Luigi Buonaguro¹ 

[1] Molecular Biology and Viral Oncogenesis Unit, Istituto Nazionale Tumori “Fond. G. Pascale”, 80131, Naples, Italy

关键词: Systems biology;    Interferon stimulated genes (ISGs);    Pattern recognition receptors (PRRs);    Innate immunity;    HCV;   

Others  :  803867
DOI  :  10.1186/1750-9378-7-7

 received in 2012-01-18, accepted in 2012-02-24,  发布年份 2012

【 摘 要 】

Hepatitis C virus (HCV) induces a chronic infection in more than two-thirds of HCV infected subjects. The inefficient innate and adaptive immune responses have been shown to play a major pathogenetic role in the development and persistence of HCV chronic infection. Several aspects of the interactions between the virus and the host immune system have been clarified and, in particular, mechanisms have been identified which underlie the ability of HCV to seize and subvert innate as well as adaptive immune responses. The present review summarizes recent findings on the interaction between HCV infection and innate immune response whose final effect is the downstream inefficient development of antigen-specific adaptive immunity, thereby contributing to virus persistence.

【 授权许可】

   
2012 Buonaguro et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Levrero M: Viral hepatitis and liver cancer: the case of hepatitis C. Oncogene 2006, 25:3834-3847.
• [2]Ferri C, Longombardo G, La CL, Greco F, Lombardini F, Cecchetti R, Cagianelli MA, Marchi S, Monti M, Zignego AL: Hepatitis C virus chronic infection as a common cause of mixed cryoglobulinaemia and autoimmune liver disease. J Intern Med 1994, 236:31-36.
• [3]Ferri C, Caracciolo F, Zignego AL, La CL, Monti M, Longombardo G, Lombardini F, Greco F, Capochiani E, Mazzoni A: Hepatitis C virus infection in patients with non-Hodgkin’s lymphoma. Br J Haematol 1994, 88:392-394.
• [4]De Re V, Caggiari L, Simula MP, De VS, Sansonno D, Dolcetti R: B-cell lymphomas associated with HCV infection. Gastroenterology 2007, 132:1205-1207.
• [5]Choo QL, Richman KH, Han JH, Berger K, Lee C, Dong C, Gallegos C, Coit D, Medina-Selby R, Barr PJ: Genetic organization and diversity of the hepatitis C virus. Proc Natl Acad Sci U S A 1991, 88:2451-2455.
• [6]Irshad M, Ansari MA, Singh A, Nag P, Raghvendra L, Singh S, Badhal SS: HCV-genotypes: a review on their origin, global status, assay system, pathogenecity and response to treatment. Hepatogastroenterology 2010, 57:1529-1538.
• [7]Fishman SL, Branch AD: The quasispecies nature and biological implications of the hepatitis C virus. Infect Genet Evol 2009, 9:1158-1167.
• [8]Han JH, Shyamala V, Richman KH, Brauer MJ, Irvine B, Urdea MS, Tekamp-Olson P, Kuo G, Choo QL, Houghton M: Characterization of the terminal regions of hepatitis C viral RNA: identification of conserved sequences in the 5′ untranslated region and poly(A) tails at the 3′ end. Proc Natl Acad Sci U S A 1991, 88:1711-1715.
• [9]Shi ST, Lai MMC: HCV 5′ and 3′UTR: When Translation Meets Replication. 2006.
• [10]Dutkiewicz M, Swiqtkowska A, Ciesiolka J: Structure and function of the non-coding regions of hepatitis C viral RNA. Postepy Biochem 2006, 52:62-71.
• [11]Suzuki T: Assembly of hepatitis C virus particles. Microbiol Immunol 2011, 55:12-18.
• [12]Choo QL, Richman KH, Han JH, Berger K, Lee C, Dong C, Gallegos C, Coit D, Medina-Selby R, Barr PJ: Genetic organization and diversity of the hepatitis C virus. Proc Natl Acad Sci U S A 1991, 88:2451-2455.
• [13]Zhang J, Randall G, Higginbottom A, Monk P, Rice CM, McKeating JA: CD81 is required for hepatitis C virus glycoprotein-mediated viral infection. J Virol 2004, 78:1448-1455.
• [14]Scarselli E, Ansuini H, Cerino R, Roccasecca RM, Acali S, Filocamo G, Traboni C, Nicosia A, Cortese R, Vitelli A: The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus. EMBO J 2002, 21:5017-5025.
• [15]Evans MJ, Von HT, Tscherne DM, Syder AJ, Panis M, Wolk B, Hatziioannou T, McKeating JA, Bieniasz PD, Rice CM: Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 2007, 446:801-805.
• [16]Zheng A, Yuan F, Li Y, Zhu F, Hou P, Li J, Song X, Ding M, Deng H: Claudin-6 and claudin-9 function as additional coreceptors for hepatitis C virus. J Virol 2007, 81:12465-12471.
• [17]Liu S, Yang W, Shen L, Turner JR, Coyne CB, Wang T: Tight junction proteins claudin-1 and occludin control hepatitis C virus entry and are downregulated during infection to prevent superinfection. J Virol 2009, 83:2011-2014.
• [18]Barth H, Rybczynska J, Patient R, Choi Y, Sapp RK, Baumert TF, Krawczynski K, Liang TJ: Both innate and adaptive immunity mediate protective immunity against hepatitis C virus infection in chimpanzees. Hepatology 2011.
• [19]Hiroishi K, Ito T, Imawari M: Immune responses in hepatitis C virus infection and mechanisms of hepatitis C virus persistence. J Gastroenterol Hepatol 2008, 23:1473-1482.
• [20]Chang KM: Immunopathogenesis of hepatitis C virus infection. Clin Liver Dis 2003, 7:89-105.
• [21]Gerlach JT, Diepolder HM, Jung MC, Gruener NH, Schraut WW, Zachoval R, Hoffmann R, Schirren CA, Santantonio T, Pape GR: Recurrence of hepatitis C virus after loss of virus-specific CD4(+) T-cell response in acute hepatitis C. Gastroenterology 1999, 117:933-941.
• [22]Shin EC, Park SH, Demino M, Nascimbeni M, Mihalik K, Major M, Veerapu NS, Heller T, Feinstone SM, Rice CM, Rehermann B: Delayed Induction, Not Impaired Recruitment of Specific CD8(+) T Cells, Causes the Late Onset of Acute Hepatitis C. Gastroenterology 2011.
• [23]Hiroishi K, Ito T, Imawari M: Immune responses in hepatitis C virus infection and mechanisms of hepatitis C virus persistence. J Gastroenterol Hepatol 2008, 23:1473-1482.
• [24]Banchereau J, Steinman RM: Dendritic cells and the control of immunity. Nature 1998, 392:245-252.
• [25]Siegal FP, Kadowaki N, Shodell M, Fitzgerald-Bocarsly PA, Shah K, Ho S, Antonenko S, Liu YJ: The nature of the principal type 1 interferon-producing cells in human blood. Science 1999, 284:1835-1837.
• [26]Matsui T, Connolly JE, Michnevitz M, Chaussabel D, Yu CI, Glaser C, Tindle S, Pypaert M, Freitas H, Piqueras B, Banchereau J, Palucka AK: CD2 distinguishes two subsets of human plasmacytoid dendritic cells with distinct phenotype and functions. J Immunol 2009, 182:6815-6823.
• [27]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.
• [28]Kanto T, Hayashi N, Takehara T, Tatsumi T, Kuzushita N, Ito A, Sasaki Y, Kasahara A, Hori M: Impaired allostimulatory capacity of peripheral blood dendritic cells recovered from hepatitis C virus-infected individuals. J Immunol 1999, 162:5584-5591.
• [29]Kanto T, Inoue M, Miyatake H, Sato A, Sakakibara M, Yakushijin T, Oki C, Itose I, Hiramatsu N, Takehara T, Kasahara A, Hayashi N: 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 2004, 190:1919-1926.
• [30]Kadowaki N, Ho S, Antonenko S, Malefyt RW, Kastelein RA, Bazan F, Liu YJ: Subsets of human dendritic cell precursors express different toll-like receptors and respond to different microbial antigens. J Exp Med 2001, 194:863-869.
• [31]Heufler C, Koch F, Stanzl U, Topar G, Wysocka M, Trinchieri G, Enk A, Steinman RM, Romani N, Schuler G: Interleukin-12 is produced by dendritic cells and mediates T helper 1 development as well as interferon-gamma production by T helper 1 cells. Eur J Immunol 1996, 26:659-668.
• [32]Pape GR, Gerlach TJ, Diepolder HM, Gruner N, Jung M, Santantonio T: Role of the specific T-cell response for clearance and control of hepatitis C virus. J Viral Hepat 1999, 6(Suppl 1):36-40.
• [33]Wertheimer AM, Bakke A, Rosen HR: Direct enumeration and functional assessment of circulating dendritic cells in patients with liver disease. Hepatology 2004, 40:335-345.
• [34]Kanto T, Inoue M, Miyatake H, Sato A, Sakakibara M, Yakushijin T, Oki C, Itose I, Hiramatsu N, Takehara T, Kasahara A, Hayashi N: 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 2004, 190:1919-1926.
• [35]Chan SH, Perussia B, Gupta JW, Kobayashi M, Pospisil M, Young HA, Wolf SF, Young D, Clark SC, Trinchieri G: Induction of interferon gamma production by natural killer cell stimulatory factor: characterization of the responder cells and synergy with other inducers. J Exp Med 1991, 173:869-879.
• [36]Khakoo SI, Thio CL, Martin MP, Brooks CR, Gao X, Astemborski J, Cheng J, Goedert JJ, Vlahov D, Hilgartner M, Cox S, Little AM, Alexander GJ, Cramp ME, O’Brien SJ, Rosenberg WM, Thomas DL, Carrington M: HLA and NK cell inhibitory receptor genes in resolving hepatitis C virus infection. Science 2004, 305:872-874.
• [37]Ahlenstiel G, Martin MP, Gao X, Carrington M, Rehermann B: Distinct KIR/HLA compound genotypes affect the kinetics of human antiviral natural killer cell responses. J Clin Invest 2008, 118:1017-1026.
• [38]Hiroishi K, Ito T, Imawari M: Immune responses in hepatitis C virus infection and mechanisms of hepatitis C virus persistence. J Gastroenterol Hepatol 2008, 23:1473-1482.
• [39]Parker GA, Picut CA: Liver immunobiology. Toxicol Pathol 2005, 33:52-62.
• [40]Akira S, Hemmi H: Recognition of pathogen-associated molecular patterns by TLR family. Immunol Lett 2003, 85:85-95.
• [41]Saito T, Gale M Jr: Principles of intracellular viral recognition. Curr Opin Immunol 2007, 19:17-23.
• [42]Saito T, Gale M Jr: Regulation of innate immunity against hepatitis C virus infection. Hepatol Res 2008, 38:115-122.
• [43]Saito T, Hirai R, Loo YM, Owen D, Johnson CL, Sinha SC, Akira S, Fujita T, Gale M Jr: Regulation of innate antiviral defenses through a shared repressor domain in RIG-I and LGP2. Proc Natl Acad Sci U S A 2007, 104:582-587.
• [44]Eksioglu EA, Zhu H, Bayouth L, Bess J, Liu HY, Nelson DR, Liu C: Characterization of HCV Interactions with Toll-Like Receptors and RIG-I in Liver Cells. PLoS One 2011, 6:e21186.
• [45]Franchi L, McDonald C, Kanneganti TD, Amer A, Nunez G: Nucleotide-binding oligomerization domain-like receptors: intracellular pattern recognition molecules for pathogen detection and host defense. J Immunol 2006, 177:3507-3513.
• [46]Imler JL, Hoffmann JA: Toll and Toll-like proteins: an ancient family of receptors signaling infection. Rev Immunogenet 2000, 2:294-304.
• [47]Tsan MF: Toll-like receptors, inflammation and cancer. Semin Cancer Biol 2006, 16:32-37.
• [48]Takeda K, Kaisho T, Akira S: Toll-like receptors. Annu Rev Immunol. 2003, 21:335-376.
• [49]Tsan MF: Toll-like receptors, inflammation and cancer. Semin Cancer Biol 2006, 16:32-37.
• [50]Kopp E, Medzhitov R: Recognition of microbial infection by Toll-like receptors. Curr Opin Immunol 2003, 15:396-401.
• [51]Dolganiuc A, Garcia C, Kodys K, Szabo G: Distinct Toll-like receptor expression in monocytes and T cells in chronic HCV infection. World J Gastroenterol 2006, 12:1198-1204.
• [52]Feldmann G, Nischalke HD, Nattermann J, Banas B, Berg T, Teschendorf C, Schmiegel W, Duhrsen U, Halangk J, Iwan A, Sauerbruch T, Caselmann WH, Spengler U: Induction of interleukin-6 by hepatitis C virus core protein in hepatitis C-associated mixed cryoglobulinemia and B-cell non-Hodgkin’s lymphoma. Clin Cancer Res 2006, 12:4491-4498.
• [53]Chiron D, Bekeredjian-Ding I, Pellat-Deceunynck C, Bataille R, Jego G: Toll-like receptors: lessons to learn from normal and malignant human B cells. Blood 2008, 112:2205-2213.
• [54]Tsan MF: Toll-like receptors, inflammation and cancer. Semin Cancer Biol 2006, 16:32-37.
• [55]Akira S, Takeda K: Toll-like receptor signalling. Nat Rev Immunol 2004, 4:499-511.
• [56]Takeda K, Akira S: TLR signaling pathway. Semin Immunol 2004, 16:3-9.
• [57]Tsan MF: Toll-like receptors, inflammation and cancer. Semin Cancer Biol 2006, 16:32-37.
• [58]Yamamoto M, Sato S, Hemmi H, Sanjo H, Uematsu S, Kaisho T, Hoshino K, Takeuchi O, Kobayashi M, Fujita T, Takeda K, Akira S: Essential role for TIRAP in activation of the signalling cascade shared by TLR2 and TLR4. Nature 2002, 420:324-329.
• [59]Yamamoto M, Sato S, Hemmi H, Hoshino K, Kaisho T, Sanjo H, Takeuchi O, Sugiyama M, Okabe M, Takeda K, Akira S: Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 2003, 301:640-643.
• [60]Gitlin L, Barchet W, Gilfillan S, Cella M, Beutler B, Flavell RA, Diamond MS, Colonna M: Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus. Proc Natl Acad Sci U S A 2006, 103:8459-8464.
• [61]Yoneyama M, Fujita T: RIG-I: critical regulator for virus-induced innate immunity. Tanpakushitsu Kakusan Koso 2004, 49:2571-2578.
• [62]Breiman A, Grandvaux N, Lin R, Ottone C, Akira S, Yoneyama M, Fujita T, Hiscott J, Meurs EF: 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.
• [63]Foy E, Li K, Sumpter R Jr, Loo YM, Johnson CL, Wang C, Fish PM, Yoneyama M, Fujita T, Lemon SM, Gale M Jr: Control of antiviral defenses through hepatitis C virus disruption of retinoic acid-inducible gene-I signaling. Proc Natl Acad Sci U S A 2005, 102:2986-2991.
• [64]Sumpter R Jr, Loo YM, Foy E, Li K, Yoneyama M, Fujita T, Lemon SM, Gale M Jr: Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. J Virol 2005, 79:2689-2699.
• [65]Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, Matsui K, Uematsu S, Jung A, Kawai T, Ishii KJ, Yamaguchi O, Otsu K, Tsujimura T, Koh CS, Reis e Sousa , Matsuura Y, Fujita T, Akira S: Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006, 441:101-105.
• [66]Yoneyama M, Kikuchi M, Matsumoto K, Imaizumi T, Miyagishi M, Taira K, Foy E, Loo YM, Gale M Jr, Akira S, Yonehara S, Kato A, Fujita T: Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J Immunol 2005, 175:2851-2858.
• [67]Saito T, Hirai R, Loo YM, Owen D, Johnson CL, Sinha SC, Akira S, Fujita T, Gale M Jr: Regulation of innate antiviral defenses through a shared repressor domain in RIG-I and LGP2. Proc Natl Acad Sci U S A 2007, 104:582-587.
• [68]Venkataraman T, Valdes M, Elsby R, Kakuta S, Caceres G, Saijo S, Iwakura Y, Barber GN: Loss of DExD/H box RNA helicase LGP2 manifests disparate antiviral responses. J Immunol 2007, 178:6444-6455.
• [69]Kawai T, Akira S: Toll-like receptor and RIG-I-like receptor signaling. Ann N Y Acad Sci 2008, 1143:1-20.
• [70]Kawai T, Akira S: Toll-like receptor and RIG-I-like receptor signaling. Ann N Y Acad Sci 2008, 1143:1-20.
• [71]Bigger CB, Brasky KM, Lanford RE: DNA microarray analysis of chimpanzee liver during acute resolving hepatitis C virus infection. J Virol 2001, 75:7059-7066.
• [72]Chen L, Borozan I, Feld J, Sun J, Tannis LL, Coltescu C, Heathcote J, Edwards AM, McGilvray ID: Hepatic gene expression discriminates responders and nonresponders in treatment of chronic hepatitis C viral infection. Gastroenterology 2005, 128:1437-1444.
• [73]Guo JT, Sohn JA, Zhu Q, Seeger C: Mechanism of the interferon alpha response against hepatitis C virus replicons. Virology 2004, 325:71-81.
• [74]Taylor DR, Puig M, Darnell ME, Mihalik K, Feinstone SM: New antiviral pathway that mediates hepatitis C virus replicon interferon sensitivity through ADAR1. J Virol 2005, 79:6291-6298.
• [75]Wang C, Pflugheber J, Sumpter R Jr, Sodora DL, Hui D, Sen GC, Gale M Jr: Alpha interferon induces distinct translational control programs to suppress hepatitis C virus RNA replication. J Virol 2003, 77:3898-3912.
• [76]Hui DJ, Bhasker CR, Merrick WC, Sen GC: Viral stress-inducible protein p56 inhibits translation by blocking the interaction of eIF3 with the ternary complex eIF2.GTP.Met-tRNAi. J Biol Chem 2003, 278:39477-39482.
• [77]Pflugheber J, Fredericksen B, Sumpter R Jr, Wang C, Ware F, Sodora DL, Gale M Jr: Regulation of PKR and IRF-1 during hepatitis C virus RNA replication. Proc Natl Acad Sci U S A 2002, 99:4650-4655.
• [78]Wang C, Pflugheber J, Sumpter R Jr, Sodora DL, Hui D, Sen GC, Gale M Jr: Alpha interferon induces distinct translational control programs to suppress hepatitis C virus RNA replication. J Virol 2003, 77:3898-3912.
• [79]Agarwal SK, Wu M, Livingston CK, Parks DH, Mayes MD, Arnett FC, Tan FK: Toll-like receptor 3 upregulation by type I interferon in healthy and scleroderma dermal fibroblasts. Arthritis Res Ther 2011, 13:R3. BioMed Central Full Text
• [80]Lin W, Kim SS, Yeung E, Kamegaya Y, Blackard JT, Kim KA, Holtzman MJ, Chung RT: Hepatitis C virus core protein blocks interferon signaling by interaction with the STAT1 SH2 domain. J Virol 2006, 80:9226-9235.
• [81]Foy E, Li K, Sumpter R Jr, Loo YM, Johnson CL, Wang C, Fish PM, Yoneyama M, Fujita T, Lemon SM, Gale M Jr: Control of antiviral defenses through hepatitis C virus disruption of retinoic acid-inducible gene-I signaling. Proc Natl Acad Sci U S A 2005, 102:2986-2991.
• [82]Lin W, Kim SS, Yeung E, Kamegaya Y, Blackard JT, Kim KA, Holtzman MJ, Chung RT: Hepatitis C virus core protein blocks interferon signaling by interaction with the STAT1 SH2 domain. J Virol 2006, 80:9226-9235.
• [83]Bode JG, Ludwig S, Ehrhardt C, Albrecht U, Erhardt A, Schaper F, Heinrich PC, Haussinger D: IFN-alpha antagonistic activity of HCV core protein involves induction of suppressor of cytokine signaling-3. FASEB J 2003, 17:488-490.
• [84]Heim MH, Moradpour D, Blum HE: Expression of hepatitis C virus proteins inhibits signal transduction through the Jak-STAT pathway. J Virol 1999, 73:8469-8475.
• [85]Polyak SJ, Khabar KS, Paschal DM, Ezelle HJ, Duverlie G, Barber GN, Levy DE, Mukaida N, Gretch DR: Hepatitis C virus nonstructural 5A protein induces interleukin-8, leading to partial inhibition of the interferon-induced antiviral response. J Virol 2001, 75:6095-6106.
• [86]Gale MJ Jr, Korth MJ, Tang NM, Tan SL, Hopkins DA, Dever TE, Polyak SJ, Gretch DR, Katze MG: Evidence that hepatitis C virus resistance to interferon is mediated through repression of the PKR protein kinase by the nonstructural 5A protein. Virology 1997, 230:217-227.
• [87]Taylor DR, Shi ST, Romano PR, Barber GN, Lai MM: Inhibition of the interferon-inducible protein kinase PKR by HCV E2 protein. Science 1999, 285:107-110.
• [88]Ahlenstiel G, Rehermann B: Hepatitis C virus and the threshold of natural killer cell inhibition. Hepatology 2005, 41:675-677.
• [89]Tseng CT, Klimpel GR: Binding of the hepatitis C virus envelope protein E2 to CD81 inhibits natural killer cell functions. J Exp Med 2002, 195:43-49.
• [90]Crotta S, Stilla A, Wack A, D’Andrea A, Nuti S, D’Oro U, Mosca M, Filliponi F, Brunetto RM, Bonino F, Abrignani S, Valiante NM: Inhibition of natural killer cells through engagement of CD81 by the major hepatitis C virus envelope protein. J Exp Med 2002, 195:35-41.
• [91]Yoon JC, Shiina M, Ahlenstiel G, Rehermann B: Natural killer cell function is intact after direct exposure to infectious hepatitis C virions. Hepatology 2009, 49:12-21.
• [92]Herzer K, Falk CS, Encke J, Eichhorst ST, Ulsenheimer A, Seliger B, Krammer PH: Upregulation of major histocompatibility complex class I on liver cells by hepatitis C virus core protein via p53 and TAP1 impairs natural killer cell cytotoxicity. J Virol 2003, 77:8299-8309.
• [93]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.
• [94]Decalf J, Fernandes S, Longman R, Ahloulay M, Audat F, Lefrerre F, Rice CM, Pol S, Albert ML: Plasmacytoid dendritic cells initiate a complex chemokine and cytokine network and are a viable drug target in chronic HCV patients. J Exp Med 2007, 204:2423-2437.
• [95]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.
• [96]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.
• [97]Yoon JC, Shiina M, Ahlenstiel G, Rehermann B: Natural killer cell function is intact after direct exposure to infectious hepatitis C virions. Hepatology 2009, 49:12-21.
• [98]Auffermann-Gretzinger S, Keeffe EB, Levy S: Impaired dendritic cell maturation in patients with chronic, but not resolved, hepatitis C virus infection. Blood 2001, 97:3171-3176.
• [99]Dolganiuc A, Kodys K, Kopasz A, Marshall C, Do T, Romics L Jr, Mandrekar P, Zapp M, Szabo G: Hepatitis C virus core and nonstructural protein 3 proteins induce pro- and anti-inflammatory cytokines and inhibit dendritic cell differentiation. J Immunol 2003, 170:5615-5624.
• [100]Kanto T, Inoue M, Miyatake H, Sato A, Sakakibara M, Yakushijin T, Oki C, Itose I, Hiramatsu N, Takehara T, Kasahara A, Hayashi N: 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 2004, 190:1919-1926.
• [101]Kanto T, Hayashi N, Takehara T, Tatsumi T, Kuzushita N, Ito A, Sasaki Y, Kasahara A, Hori M: Impaired allostimulatory capacity of peripheral blood dendritic cells recovered from hepatitis C virus-infected individuals. J Immunol 1999, 162:5584-5591.
• [102]Bain C, Fatmi A, Zoulim F, Zarski JP, Trepo C, Inchauspe G: Impaired allostimulatory function of dendritic cells in chronic hepatitis C infection. Gastroenterology 2001, 120:512-524.
• [103]Longman RS, Talal AH, Jacobson IM, Albert ML, Rice CM: Presence of functional dendritic cells in patients chronically infected with hepatitis C virus. Blood 2004, 103:1026-1029.
• [104]Barnaba V: Hepatitis C virus infection: a “liaison a trois” amongst the virus, the host, and chronic low-level inflammation for human survival. J Hepatol 2010, 53:752-761.
• [105]Albert ML, Decalf J, Pol S: Plasmacytoid dendritic cells move down on the list of suspects: in search of the immune pathogenesis of chronic hepatitis C. J Hepatol 2008, 49:1069-1078.
• [106]Potti A, Mukherjee S, Petersen R, Dressman HK, Bild A, Koontz J, Kratzke R, Watson MA, Kelley M, Ginsburg GS, West M, Harpole DH Jr, Nevins JR: A genomic strategy to refine prognosis in early-stage non-small-cell lung cancer. N Engl J Med 2006, 355:570-580.
• [107]Alizadeh AA, Staudt LM: Genomic-scale gene expression profiling of normal and malignant immune cells. Curr Opin Immunol 2000, 12:219-225.
• [108]Sorlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, Hastie T, Eisen MB, van de RM, Jeffrey SS, Thorsen T, Quist H, Matese JC, Brown PO, Botstein D, Eystein LP, Borresen-Dale AL: Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A 2001, 98:10869-10874.
• [109]Chaussabel D, Quinn C, Shen J, Patel P, Glaser C, Baldwin N, Stichweh D, Blankenship D, Li L, Munagala I, Bennett L, Allantaz F, Mejias A, Ardura M, Kaizer E, Monnet L, Allman W, Randall H, Johnson D, Lanier A, Punaro M, Wittkowski KM, White P, Fay J, Klintmalm G, Ramilo O, Palucka AK, Banchereau J, Pascual V: A modular analysis framework for blood genomics studies: application to systemic lupus erythematosus. Immunity 2008, 29:150-164.
• [110]Ramilo O, Allman W, Chung W, Mejias A, Ardura M, Glaser C, Wittkowski KM, Piqueras B, Banchereau J, Palucka AK, Chaussabel D: Gene expression patterns in blood leukocytes discriminate patients with acute infections. Blood 2007, 109:2066-2077.
• [111]Buonaguro L, Petrizzo A, Tornesello M, Napolitano M, Martorelli D, Castello G, Beneduce G, De RA, Perrella O, Romagnoli L, Sousa V, De RV, Dolcetti R, Buonaguro FM: Immune signatures in human PBMCs of idiotypic vaccine for HCV-related lymphoproliferative disorders. J Transl Med 2010, 8:18. BioMed Central Full Text
• [112]Buonaguro L, Pulendran B: Immunogenomics and systems biology of vaccines. Immunol Rev 2011, 239:197-208.
• [113]Pulendran B, Li S, Nakaya HI: Systems vaccinology. Immunity 2010, 33:516-529.
• [114]Folkers ME, Delker DA, Maxwell CI, Nelson CA, Schwartz JJ, Nix DA, Hagedorn CH: ENCODE tiling array analysis identifies differentially expressed annotated and novel 5′ capped RNAs in hepatitis C infected liver. PLoS One 2011, 6:e14697.
• [115]Itsui Y, Sakamoto N, Kurosaki M, Kanazawa N, Tanabe Y, Koyama T, Takeda Y, Nakagawa M, Kakinuma S, Sekine Y, Maekawa S, Enomoto N, Watanabe M: Expressional screening of interferon-stimulated genes for antiviral activity against hepatitis C virus replication. J Viral Hepat 2006, 13:690-700.
• [116]Wietzke-Braun P, Maouzi AB, Manhardt LB, Bickeboller H, Ramadori G, Mihm S: Interferon regulatory factor-1 promoter polymorphism and the outcome of hepatitis C virus infection. Eur J Gastroenterol Hepatol 2006, 18:991-997.
• [117]Nisole S, Stoye JP, Saib A: TRIM family proteins: retroviral restriction and antiviral defence. Nat Rev Microbiol 2005, 3:799-808.
• [118]Vlad G, Piazza F, Colovai A, Cortesini R, Della PF, Suciu-Foca N, Manavalan JS: Interleukin-10 induces the upregulation of the inhibitory receptor ILT4 in monocytes from HIV positive individuals. Hum Immunol 2003, 64:483-489.
• [119]Chang CC, Liu Z, Vlad G, Qin H, Qiao X, Mancini DM, Marboe CC, Cortesini R, Suciu-Foca N: Ig-like transcript 3 regulates expression of proinflammatory cytokines and migration of activated T cells. J Immunol 2009, 182:5208-5216.
• [120]Khalid SS, Hamid S, Siddiqui AA, Qureshi A, Qureshi N: Gene profiling of early and advanced liver disease in chronic hepatitis C patients. Hepatol Int 2011.
• [121]Shackel NA, McGuinness PH, Abbott CA, Gorrell MD, McCaughan GW: Insights into the pathobiology of hepatitis C virus-associated cirrhosis: analysis of intrahepatic differential gene expression. Am J Pathol 2002, 160:641-654.
• [122]Smith MW, Yue ZN, Korth MJ, Do HA, Boix L, Fausto N, Bruix J, Carithers RL Jr, Katze MG: Hepatitis C virus and liver disease: global transcriptional profiling and identification of potential markers. Hepatology 2003, 38:1458-1467.
• [123]Bieche I, Asselah T, Laurendeau I, Vidaud D, Degot C, Paradis V, Bedossa P, Valla DC, Marcellin P, Vidaud M: Molecular profiling of early stage liver fibrosis in patients with chronic hepatitis C virus infection. Virology 2005, 332:130-144.
• [124]Khalid SS, Hamid S, Siddiqui AA, Qureshi A, Qureshi N: Gene profiling of early and advanced liver disease in chronic hepatitis C patients. Hepatol Int 2011.
• [125]Blackham S, Baillie A, Al-Hababi F, Remlinger K, You S, Hamatake R, McGarvey MJ: Gene expression profiling indicates the roles of host oxidative stress, apoptosis, lipid metabolism, and intracellular transport genes in the replication of hepatitis C virus. J Virol 2010, 84:5404-5414.
• [126]Blackham S, Baillie A, Al-Hababi F, Remlinger K, You S, Hamatake R, McGarvey MJ: Gene expression profiling indicates the roles of host oxidative stress, apoptosis, lipid metabolism, and intracellular transport genes in the replication of hepatitis C virus. J Virol 2010, 84:5404-5414.
• [127]Blackham S, Baillie A, Al-Hababi F, Remlinger K, You S, Hamatake R, McGarvey MJ: Gene expression profiling indicates the roles of host oxidative stress, apoptosis, lipid metabolism, and intracellular transport genes in the replication of hepatitis C virus. J Virol 2010, 84:5404-5414.
• [128]De Giorgi V, Monaco A, Worchech A, Tornesello M, Izzo F, Buonaguro L, Marincola FM, Wang E, Buonaguro FM: Gene profiling, biomarkers and pathways characterizing HCV-related hepatocellular carcinoma. J Transl Med 2009, 7:85. BioMed Central Full Text
• [129]Blackham S, Baillie A, Al-Hababi F, Remlinger K, You S, Hamatake R, McGarvey MJ: Gene expression profiling indicates the roles of host oxidative stress, apoptosis, lipid metabolism, and intracellular transport genes in the replication of hepatitis C virus. J Virol 2010, 84:5404-5414.
• [130]Ouchi M, Ouchi T: Role of IFI16 in DNA damage and checkpoint. Front Biosci 2008, 13:236-239.
• [131]Kwak JC, Ongusaha PP, Ouchi T, Lee SW: IFI16 as a negative regulator in the regulation of p53 and p21(Waf1). J Biol Chem 2003, 278:40899-40904.
• [132]Rosebeck S, Leaman DW: Mitochondrial localization and pro-apoptotic effects of the interferon-inducible protein ISG12a. Apoptosis 2008, 13:562-572.
• [133]Andersen JB, Strandbygard DJ, Hartmann R, Justesen J: Interaction between the 2′-5′ oligoadenylate synthetase-like protein p59 OASL and the transcriptional repressor methyl CpG-binding protein 1. Eur J Biochem 2004, 271:628-636.
• [134]Scholz C, Tampe R: The intracellular antigen transport machinery TAP in adaptive immunity and virus escape mechanisms. J Bioenerg Biomembr 2005, 37:509-515.
• [135]Herzer K, Falk CS, Encke J, Eichhorst ST, Ulsenheimer A, Seliger B, Krammer PH: Upregulation of major histocompatibility complex class I on liver cells by hepatitis C virus core protein via p53 and TAP1 impairs natural killer cell cytotoxicity. J Virol 2003, 77:8299-8309.
• [136]Chen L, Borozan I, Sun J, Guindi M, Fischer S, Feld J, Anand N, Heathcote J, Edwards AM, McGilvray ID: Cell-type specific gene expression signature in liver underlies response to interferon therapy in chronic hepatitis C infection. Gastroenterology 2010, 138:1123-1133.
• [137]Chen L, Borozan I, Feld J, Sun J, Tannis LL, Coltescu C, Heathcote J, Edwards AM, McGilvray ID: Hepatic gene expression discriminates responders and nonresponders in treatment of chronic hepatitis C viral infection. Gastroenterology 2005, 128:1437-1444.
• [138]Khalid SS, Hamid S, Siddiqui AA, Qureshi A, Qureshi N: Gene profiling of early and advanced liver disease in chronic hepatitis C patients. Hepatol Int 2011.
• [139]Blackham S, Baillie A, Al-Hababi F, Remlinger K, You S, Hamatake R, McGarvey MJ: Gene expression profiling indicates the roles of host oxidative stress, apoptosis, lipid metabolism, and intracellular transport genes in the replication of hepatitis C virus. J Virol 2010, 84:5404-5414.