Role of macrophages and monocytes in hepatitis C virus infections

World Journal of Gastroenterology

Volumn 20, Issue 11, 2014, Pages 2777-2784

  Revie, Dennis ^a   Salahuddin, Syed Zaki ^b  

^a CALIFORNIA LUTHERAN UNIVERSITY   (United States)

^b California Institute of Molecular Medicine   (United States)

Author keywords

Dendritic cells; Hepatitis C virus; Hepatitis C virus replication; Macrophages; Monocytes

Indexed keywords

GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 1BETA; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; VIRUS RNA;

ARTICLE; COGNITIVE DEFECT; CRYOGLOBULINEMIA; DENDRITIC CELL; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GENE SEQUENCE; GENETIC VARIABILITY; GENOTYPE; HEPATITIS C; HUMAN; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MACROPHAGE; MONOCYTE; POLYMERASE CHAIN REACTION; VIRUS REPLICATION; IMMUNOLOGY; MONONUCLEAR PHAGOCYTE; PHYSIOLOGY; VIROLOGY;

HEPATITIS C; HUMANS; MONONUCLEAR PHAGOCYTE SYSTEM; VIRUS REPLICATION;

EID: 84896445702     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v20.i11.2777     Document Type: Article

References (65)

1. Kita H, Mackay IR, Van De Water J, Gershwin ME. The lymphoid liver: considerations on pathways to autoimmune injury. Gastroenterology 2001; 120: 1485-1501 [PMID: 11313320 DOI: 10.1053/gast.2001.22441]
2. Dong Z, Wei H, Sun R, Tian Z. The roles of innate immune cells in liver injury and regeneration. Cell Mol Immunol 2007; 4: 241-252 [PMID: 17764614]
3. Aguzzi A, Barres BA, Bennett ML. Microglia: scapegoat, saboteur, or something else? Science 2013; 339: 156-161 [PMID: 23307732 DOI: 10.1126/science.1227901]
4. Baffy G. Kupffer cells in non-alcoholic fatty liver disease: the emerging view. J Hepatol 2009; 51: 212-223 [PMID: 19447517 DOI: 10.1016/j.jhep.2009.03.008]
5. Stienstra R, Saudale F, Duval C, Keshtkar S, Groener JE, van Rooijen N, Staels B, Kersten S, Müller M. Kupffer cells promote hepatic steatosis via interleukin-1beta-dependent suppression of peroxisome proliferator-activated receptor alpha activity. Hepatology 2010; 51: 511-522 [PMID: 20054868 DOI: 10.1002/hep.23337]
6. Ko HM, Hernandez-Prera JC, Zhu H, Dikman SH, Sidhu HK, Ward SC, Thung SN. Morphologic features of extrahepatic manifestations of hepatitis C virus infection. Clin Dev Immunol 2012; 2012: 740138 [PMID: 22919404 DOI: 10.1155/2012/740138]
7. Monaco S, Ferrari S, Gajofatto A, Zanusso G, Mariotto S. HCV-related nervous system disorders. Clin Dev Immunol 2012; 2012: 236148 [PMID: 22899946 DOI: 10.1155/2012/236148]
8. Revie D, Salahuddin SZ. Human cell types important for hepatitis C virus replication in vivo and in vitro: old assertions and current evidence. Virol J 2011; 8: 346 [PMID: 21745397 DOI: 10.1186/1743-422x-8-346]
9. Friebe P, Lohmann V, Krieger N, Bartenschlager R. Sequences in the 5' nontranslated region of hepatitis C virus required for RNA replication. J Virol 2001; 75: 12047-12057 [PMID: 11711595 DOI: 10.1128/JVI.75.24.12047-12057.2001]
10. Rijnbrand RC, Lemon SM. Internal ribosome entry site-mediated translation in hepatitis C virus replication. Curr Top Microbiol Immunol 2000; 242: 85-116 [PMID: 10592657 DOI: 10.1007/978-3-642-59605-6_5]
11. Wang C, Sarnow P, Siddiqui A. Translation of human hepatitis C virus RNA in cultured cells is mediated by an internal ribosome-binding mechanism. J Virol 1993; 67: 3338-3344 [PMID: 8388503]
12. Wang JT, Sheu JC, Lin JT, Wang TH, Chen DS. Detection of replicative form of hepatitis C virus RNA in peripheral blood mononuclear cells. J Infect Dis 1992; 166: 1167-1169 [PMID: 1328405 DOI: 10.1093/infdis/166.5.1167]
13. Qian C, Camps J, Maluenda MD, Civeira MP, Prieto J. Replication of hepatitis C virus in peripheral blood mononuclear cells. Effect of alpha-interferon therapy. J Hepatol 1992; 16: 380-383 [PMID: 1336787 DOI: 10.1016/S0168-8278(05)80674-9]
14. Bouffard P, Hayashi PH, Acevedo R, Levy N, Zeldis JB. Hepatitis C virus is detected in a monocyte/macrophage subpopulation of peripheral blood mononuclear cells of infected patients. J Infect Dis 1992; 166: 1276-1280 [PMID: 1385547 DOI: 10.1093/infdis/166.6.1276]
15. Zignego AL, Macchia D, Monti M, Thiers V, Mazzetti M, Foschi M, Maggi E, Romagnani S, Gentilini P, Bréchot C. Infection of peripheral mononuclear blood cells by hepatitis C virus. J Hepatol 1992; 15: 382-386 [PMID: 1332999 DOI: 10.1016/0168-8278(92)90073-X]
16. Sansonno D, Iacobelli AR, Cornacchiulo V, Iodice G, Dammacco F. Detection of hepatitis C virus (HCV) proteins by immunofluorescence and HCV RNA genomic sequences by non-isotopic in situ hybridization in bone marrow and peripheral blood mononuclear cells of chronically HCV-infected patients. Clin Exp Immunol 1996; 103: 414-421 [PMID: 8608640 DOI: 10.1111/j.1365-2249.1996.tb08296.x]
17. Lerat H, Rumin S, Habersetzer F, Berby F, Trabaud MA, Trépo C, Inchauspé G. In vivo tropism of hepatitis C virus genomic sequences in hematopoietic cells: influence of viral load, viral genotype, and cell phenotype. Blood 1998; 91: 3841-3849 [PMID: 9573022]
18. Laskus T, Radkowski M, Piasek A, Nowicki M, Horban A, Cianciara J, Rakela J. Hepatitis C virus in lymphoid cells of patients coinfected with human immunodeficiency virus type 1: evidence of active replication in monocytes/macrophages and lymphocytes. J Infect Dis 2000; 181: 442-448 [PMID: 10669324 DOI: 10.1086/315283]
19. Crovatto M, Pozzato G, Zorat F, Pussini E, Nascimben F, Baracetti S, Grando MG, Mazzaro C, Reitano M, Modolo ML, Martelli P, Spada A, Santini G. Peripheral blood neutrophils from hepatitis C virus-infected patients are replication sites of the virus. Haematologica 2000; 85: 356-361 [PMID: 10756359]
20. Natarajan V, Kottilil S, Hazen A, Adelsberger J, Murphy AA, Polis MA, Kovacs JA. HCV in peripheral blood mononuclear cells are predominantly carried on the surface of cells in HIV/HCV co-infected individuals. J Med Virol 2010; 82: 2032-2037 [PMID: 20981790 DOI: 10.1002/jmv.21906]
21. Matsumori A, Shimada M, Obata T. Leukocytes are the major target of hepatitis C virus infection: Possible mechanism of multiorgan involvement including the heart. CVD Prev Control 2010; 5: 51-58 [DOI: 10.1016/j.cvdpc.2010.04.005]
22. Sansonno D, Cornacchiulo V, Racanelli V, Dammacco F. In situ simultaneous detection of hepatitis C virus RNA and hepatitis C virus-related antigens in hepatocellular carcinoma. Cancer 1997; 80: 22-33 [PMID: 9210705]
23. Benkoël L, Biagini P, Dodero F, De Lamballerie X, De Micco P, Chamlian A. Immunohistochemical detection of C-100 hepatitis C virus antigen in formaldehyde-fixed paraffin-embedded liver tissue. Correlation with serum, tissue and in situ RT-PCR results. Eur J Histochem 2004; 48: 185-190 [PMID: 15208088]
24. Pham TN, King D, Macparland SA, McGrath JS, Reddy SB, Bursey FR, Michalak TI. Hepatitis C virus replicates in the same immune cell subsets in chronic hepatitis C and occult infection. Gastroenterology 2008; 134: 812-822 [PMID: 18243182 DOI: 10.1053/j.gastro.2007.12.011]
25. Sansonno D, Gesualdo L, Manno C, Schena FP, Dammacco F. Hepatitis C virus-related proteins in kidney tissue from hepatitis C virus-infected patients with cryoglobulinemic membranoproliferative glomerulonephritis. Hepatology 1997; 25: 1237-1244 [PMID: 9141444 DOI: 10.1002/hep.510250529]
26. Maggi F, Fornai C, Morrica A, Vatteroni ML, Giorgi M, Marchi S, Ciccorossi P, Bendinelli M, Pistello M. Divergent evolution of hepatitis C virus in liver and peripheral blood mononuclear cells of infected patients. J Med Virol 1999; 57: 57-63 [PMID: 9890422]
27. Okuda M, Hino K, Korenaga M, Yamaguchi Y, Katoh Y, Okita K. Differences in hypervariable region 1 quasispecies of hepatitis C virus in human serum, peripheral blood mononuclear cells, and liver. Hepatology 1999; 29: 217-222 [PMID: 9862869 DOI: 10.1002/hep.510290117]
28. Navas S, Martín J, Quiroga JA, Castillo I, Carreño V. Genetic diversity and tissue compartmentalization of the hepatitis C virus genome in blood mononuclear cells, liver, and serum from chronic hepatitis C patients. J Virol 1998; 72: 1640-1646 [PMID: 9445070]
29. Ducoulombier D, Roque-Afonso AM, Di Liberto G, Penin F, Kara R, Richard Y, Dussaix E, Féray C. Frequent compartmentalization of hepatitis C virus variants in circulating B cells and monocytes. Hepatology 2004; 39: 817-825 [PMID: 14999702 DOI: 10.1002/hep.20087]
30. Coquillard G, Patterson BK. Determination of hepatitis C virus-infected, monocyte lineage reservoirs in individuals with or without HIV coinfection. J Infect Dis 2009; 200: 947-954 [PMID: 19678757 DOI: 10.1086/605476]
31. Blight K, Trowbridge R, Rowland R, Gowans E. Detection of hepatitis C virus RNA by in situ hybridization. Liver 1992; 12: 286-289 [PMID: 1333032]
32. Radkowski M, Wilkinson J, Nowicki M, Adair D, Vargas H, Ingui C, Rakela J, Laskus T. Search for hepatitis C virus negative-strand RNA sequences and analysis of viral sequences in the central nervous system: evidence of replication. J Virol 2002; 76: 600-608 [PMID: 11752151 DOI: 10.1128/JVI.76.2.600-608.2002]
33. Forton DM, Karayiannis P, Mahmud N, Taylor-Robinson SD, Thomas HC. Identification of unique hepatitis C virus quasispecies in the central nervous system and comparative analysis of internal translational efficiency of brain, liver, and serum variants. J Virol 2004; 78: 5170-5183 [PMID: 15113899 DOI: 10.1128/JVI.78.10.5170-5183.2004]
34. Letendre S, Paulino AD, Rockenstein E, Adame A, Crews L, Cherner M, Heaton R, Ellis R, Everall IP, Grant I, Masliah E. Pathogenesis of hepatitis C virus coinfection in the brains of patients infected with HIV. J Infect Dis 2007; 196: 361-370 [PMID: 17597450 DOI: 10.1086/519285]
35. Wilkinson J, Radkowski M, Eschbacher JM, Laskus T. Activation of brain macrophages/microglia cells in hepatitis C infection. Gut 2010; 59: 1394-1400 [PMID: 20675697 DOI: 10.1136/gut.2009.199356]
36. 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 [PMID: 16534871]
37. 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 [PMID: 17845690 DOI: 10.1111/j.1440-1746.2006.04783.x]
38. -monocytes is weakly modulated as a consequence of persistent infection with the hepatitis C virus. Mol Immunol 2011; 48: 1505-1511 [PMID: 21531464 DOI: 10.1016/j.molimm.2011.04.008]
39. Bain C, Fatmi A, Zoulim F, Zarski JP, Trépo C, Inchauspé G. Impaired allostimulatory function of dendritic cells in chronic hepatitis C infection. Gastroenterology 2001; 120: 512-524 [PMID: 11159892]
40. Goutagny N, Fatmi A, De Ledinghen V, Penin F, Couzigou P, Inchauspé G, Bain C. Evidence of viral replication in circulating dendritic cells during hepatitis C virus infection. J Infect Dis 2003; 187: 1951-1958 [PMID: 12792872]
41. Goutagny N, Vieux C, Decullier E, Ligeoix B, Epstein A, Trepo C, Couzigou P, Inchauspe G, Bain C. Quantification and functional analysis of plasmacytoid dendritic cells in patients with chronic hepatitis C virus infection. J Infect Dis 2004; 189: 1646-1655 [PMID: 15116301 DOI: 10.1086/383248]
42. Gelderblom HC, Nijhuis LE, de Jong EC, te Velde AA, Pajkrt D, Reesink HW, Beld MG, van Deventer SJ, Jansen PL. Monocyte-derived dendritic cells from chronic HCV patients are not infected but show an immature phenotype and aberrant cytokine profile. Liver Int 2007; 27: 944-953 [PMID: 17696933 DOI: 10.1111/j.1478-3231.2007.01507.x]
43. Ryan EJ, O'Farrelly C. The affect of chronic hepatitis C infection on dendritic cell function: a summary of the experimental evidence. J Viral Hepat 2011; 18: 601-607 [PMID: 21794024 DOI: 10.1111/j.1365-2893.2011.01453.x]
44. Palmer BA, Moreau I, Levis J, Harty C, Crosbie O, Kenny-Walsh E, Fanning LJ. Insertion and recombination events at hypervariable region 1 over 9.6 years of hepatitis C virus chronic infection. J Gen Virol 2012; 93: 2614-2624 [PMID: 22971825 DOI: 10.1099/vir.0.045344-0]
45. Caussin-Schwemling C, Schmitt C, Stoll-Keller F. Study of the infection of human blood derived monocyte/macrophages with hepatitis C virus in vitro. J Med Virol 2001; 65: 14-22 [PMID: 11505438]
46. Royer C, Steffan AM, Navas MC, Fuchs A, Jaeck D, Stoll-Keller F. A study of susceptibility of primary human Kupffer cells to hepatitis C virus. J Hepatol 2003; 38: 250-256 [PMID: 12586289]
47. Radkowski M, Bednarska A, Horban A, Stanczak J, Wilkinson J, Adair DM, Nowicki M, Rakela J, Laskus T. Infection of primary human macrophages with hepatitis C virus in vitro: induction of tumour necrosis factor-alpha and interleukin 8. J Gen Virol 2004; 85: 47-59 [PMID: 14718619]
48. Laskus T, Radkowski M, Jablonska J, Kibler K, Wilkinson J, Adair D, Rakela J. Human immunodeficiency virus facilitates infection/replication of hepatitis C virus in native human macrophages. Blood 2004; 103: 3854-3859 [PMID: 14739225]
49. el-Awady MK, Tabll AA, el-Redwan RM, Youssef S, Omran MH, Thakeb F, el-Demellawy M. Flow cytometric detection of hepatitis C virus antigens in infected peripheral blood leukocytes: binding and entry. World J Gastroenterol 2005; 11: 5203-5208 [PMID: 16127753]
50. Ponzetto A, Gennero L, Cutufia M, Beltramo T, Enrietto M, Pescarmona P, Pugliese A. Effect of HCV infection on THP-1 monocytoid cells. Cell Biochem Funct 2005; 23: 347-352 [PMID: 15515125 DOI: 10.1002/cbf.1158]
51. Lau DT, Negash A, Chen J, Crochet N, Sinha M, Zhang Y, Guedj J, Holder S, Saito T, Lemon SM, Luxon BA, Perelson AS, Gale M. Innate immune tolerance and the role of kupffer cells in differential responses to interferon therapy among patients with HCV genotype 1 infection. Gastroenterology 2013; 144: 402-413. e12 [PMID: 23123437 DOI: 10.1053/j.gastro.2012.10.044]
52. Negash AA, Ramos HJ, Crochet N, Lau DT, Doehle B, Papic N, Delker DA, Jo J, Bertoletti A, Hagedorn CH, Gale M. IL-1β production through the NLRP3 inflammasome by hepatic macrophages links hepatitis C virus infection with liver inflammation and disease. PLoS Pathog 2013; 9: e1003330 [PMID: 23633957 DOI: 10.1371/journal.ppat.1003330]
53. Navas MC, Fuchs A, Schvoerer E, Bohbot A, Aubertin AM, Stoll-Keller F. Dendritic cell susceptibility to hepatitis C virus genotype 1 infection. J Med Virol 2002; 67: 152-161 [PMID: 11992576 DOI: 10.1002/jmv.2204]
54. Lambotin M, Baumert TF, Barth H. Distinct intracellular trafficking of hepatitis C virus in myeloid and plasmacytoid dendritic cells. J Virol 2010; 84: 8964-8969 [PMID: 20573834 DOI: 10.1128/JVI.00517-10]
55. Revie D, Braich RS, Bayles D, Chelyapov N, Khan R, Geer C, Reisman R, Kelley AS, Prichard JG, Salahuddin SZ. Transmission of human hepatitis C virus from patients in secondary cells for long term culture. Virol J 2005; 2: 37 [PMID: 15840164 DOI: 10.1186/1743-422X-2-37]
56. Revie D, Alberti MO, Braich RS, Chelyapov N, Bayles D, Prichard JG, Salahuddin SZ. Analysis of in vitro replicated human hepatitis C virus (HCV) for the determination of genotypes and quasispecies. Virol J 2006; 3: 81 [PMID: 17010197 DOI: 10.1186/1743-422X-3-81]
57. Revie D, Alberti MO, Braich RS, Bayles D, Prichard JG, Salahuddin SZ. Discovery of significant variants containing large deletions in the 5'UTR of human hepatitis C virus (HCV). Virol J 2006; 3: 82 [PMID: 17010198 DOI: 10.1186/1743-422X-3-82]
58. Revie D, Alberti MO, Prichard JG, Kelley AS, Salahuddin SZ. Analysis of the 5'UTR of HCV genotype 3 grown in vitro in human B cells, T cells, and macrophages. Virol J 2010; 7: 155 [PMID: 20626910 DOI: 10.1186/1743-422X-7-155]
59. Welsch S, Groot F, Kräusslich HG, Keppler OT, Sattentau QJ. Architecture and regulation of the HIV-1 assembly and holding compartment in macrophages. J Virol 2011; 85: 7922-7927 [PMID: 21613397 DOI: 10.1128/jvi.00834-11]
60. Farnik H, Mihm U, Zeuzem S. Optimal therapy in genotype 1 patients. Liver Int 2009; 29 Suppl 1: 23-30 [PMID: 19207963 DOI: 10.1111/j.1478-3231.2008.01969.x]
61. NIH Consensus Statement on Management of Hepatitis C: 2002. NIH Consens State Sci Statements 2002; 19: 1-46 [PMID: 14768714]
62. Di Liberto G, Roque-Afonso AM, Kara R, Ducoulombier D, Fallot G, Samuel D, Feray C. Clinical and therapeutic implications of hepatitis C virus compartmentalization. Gastroenterology 2006; 131: 76-84 [PMID: 16831592]
63. Sansonno D, Tucci FA, Lauletta G, De Re V, Montrone M, Troiani L, Sansonno L, Dammacco F. Hepatitis C virus productive infection in mononuclear cells from patients with cryoglobulinaemia. Clin Exp Immunol 2007; 147: 241-248 [PMID: 17223964]
64. Boddi M, Abbate R, Chellini B, Giusti B, Giannini C, Pratesi G, Rossi L, Pratesi C, Gensini GF, Paperetti L, Zignego AL. Hepatitis C virus RNA localization in human carotid plaques. J Clin Virol 2010; 47: 72-75 [PMID: 19896417]
65. Kurokawa M, Hidaka T, Sasaki H, Nishikata I, Morishita K, Setoyama M. Analysis of hepatitis C virus (HCV) RNA in the lesions of lichen planus in patients with chronic hepatitis C: detection of anti-genomic-as well as genomic-strand HCV RNAs in lichen planus lesions. J Dermatol Sci 2003; 32: 65-70 [PMID: 12788531]