Skip to main content
Top
Published in: Virology Journal 1/2011

Open Access 01-12-2011 | Research

Increased HCMV seroprevalence in patients with hepatocellular carcinoma

Authors: Quentin Lepiller, Manoj K Tripathy, Vincent Di Martino, Bernadette Kantelip, Georges Herbein

Published in: Virology Journal | Issue 1/2011

Login to get access

Abstract

Background

Hepatocellular carcinoma (HCC) is the most common primary liver cancer, usually arising after years of chronic liver inflammation that could result from viral infections such as hepatitis B virus (HBV) and hepatitic C virus (HCV) infections. Human cytomegalovirus (HCMV) infects primary human hepatocytes and remains an important cause of morbidity in immunocompromised persons where it may manifest as symptomatic end-organ disease including hepatitis. The goal of the present study was to determine a potential correlation between HCMV infection and the appearance of HCC.

Methods

First, we analyzed the seroprevalence of HCMV in a cohort of 11,318 patients hospitalized between 2003 and 2009 in different departments of a French University Hospital. Second, we studied HCMV seroprevalence in a cohort of 190 subjects who were stratified on the basis of age, gender, HCC, cirrhosis (Cir), and the exposition to hepatotropic viruses (HCV, HBV). We further determined whether HCMV DNA was present specifically in tumour area in liver biopsies from HCC-positive patients by using nested PCR.

Results

We found that the HCMV seroprevalence was high in the Hepatology department. The HCMV seroprevalence was significantly higher in patients infected with HCV and/or HBV than in patients who were not infected by those later viruses (76.2% versus 56.5%, p < 0.001). The HCMV seroprevalence was significantly higher in patients with HCC (74%) and lower in patients without HCC (54% for HCC-/Cir+ patients, 57% for HCC-/Cir- subjects). We observed a positive correlation between serum IL-6 levels and HCMV seroprevalence in cirrhotic patients, but not in HCC patients. Serum IL-6 levels correlated positively with C-reactive protein (CRP) levels. Preliminary histological studies from liver biopsies from HCC-positive patients highlighted that HCMV DNA can be detected in tumour area of some of the patients studied.

Conclusions

Our results indicate that HCMV seroprevalence in patients with HCC is significantly higher than in patients without HCC, is positively correlated with serum IL-6 levels in cirrhotic patients, and is positively associated with the presence of other hepatotropic viruses such as HCV and HBV.
Appendix
Available only for authorised users
Literature
1.
go back to reference Khoruts A, Stahnke L, McClain CJ, Logan G, Allen JI: Circulating tumor necrosis factor, interleukin-1 and interleukin-6 concentrations in chronic alcoholic patients. Hepatology 1991, 13: 267-276.CrossRefPubMed Khoruts A, Stahnke L, McClain CJ, Logan G, Allen JI: Circulating tumor necrosis factor, interleukin-1 and interleukin-6 concentrations in chronic alcoholic patients. Hepatology 1991, 13: 267-276.CrossRefPubMed
2.
go back to reference Kakumu S, Shinagawa T, Ishikawa T, Yoshioka K, Wakita T, Ito Y, Takayanagi M, Ida N: Serum interleukin 6 levels in patients with chronic hepatitis B. Am J Gastroenterol 1991, 86: 1804-1808.PubMed Kakumu S, Shinagawa T, Ishikawa T, Yoshioka K, Wakita T, Ito Y, Takayanagi M, Ida N: Serum interleukin 6 levels in patients with chronic hepatitis B. Am J Gastroenterol 1991, 86: 1804-1808.PubMed
3.
go back to reference Malaguarnera M, Di Fazio I, Laurino A, Ferlito L, Romano M, Trovato BA: Serum interleukin 6 concentrations in chronic hepatitis C patients before and after interferon-alpha treatment. Int J Clin Pharmacol Ther 1997, 35: 385-388.PubMed Malaguarnera M, Di Fazio I, Laurino A, Ferlito L, Romano M, Trovato BA: Serum interleukin 6 concentrations in chronic hepatitis C patients before and after interferon-alpha treatment. Int J Clin Pharmacol Ther 1997, 35: 385-388.PubMed
4.
go back to reference Soresi M, Giannitrapani L, D'Antona F, Florena AM, La Spada E, Terranova A, Cervello M, D'Alessandro N, Montalto G: Interleukin-6 and its soluble receptor in patients with liver cirrhosis and hepatocellular carcinoma. World J Gastroenterol 2006, 12: 2563-2568.PubMedCentralPubMed Soresi M, Giannitrapani L, D'Antona F, Florena AM, La Spada E, Terranova A, Cervello M, D'Alessandro N, Montalto G: Interleukin-6 and its soluble receptor in patients with liver cirrhosis and hepatocellular carcinoma. World J Gastroenterol 2006, 12: 2563-2568.PubMedCentralPubMed
5.
go back to reference Malaguarnera M, Di Fazio I, Laurino A, Romeo MA, Giugno I, Trovato BA: [Role of interleukin 6 in hepatocellular carcinoma]. Bull Cancer 1996, 83: 379-384.PubMed Malaguarnera M, Di Fazio I, Laurino A, Romeo MA, Giugno I, Trovato BA: [Role of interleukin 6 in hepatocellular carcinoma]. Bull Cancer 1996, 83: 379-384.PubMed
6.
go back to reference Naugler WE, Karin M: The wolf in sheep's clothing: the role of interleukin-6 in immunity, inflammation and cancer. Trends Mol Med 2008, 14: 109-119. 10.1016/j.molmed.2007.12.007CrossRefPubMed Naugler WE, Karin M: The wolf in sheep's clothing: the role of interleukin-6 in immunity, inflammation and cancer. Trends Mol Med 2008, 14: 109-119. 10.1016/j.molmed.2007.12.007CrossRefPubMed
7.
go back to reference Park EJ, Lee JH, Yu GY, He G, Ali SR, Holzer RG, Osterreicher CH, Takahashi H, Karin M: Dietary and genetic obesity promote liver inflammation and tumorigenesis by enhancing IL-6 and TNF expression. Cell 2010, 140: 197-208. 10.1016/j.cell.2009.12.052PubMedCentralCrossRefPubMed Park EJ, Lee JH, Yu GY, He G, Ali SR, Holzer RG, Osterreicher CH, Takahashi H, Karin M: Dietary and genetic obesity promote liver inflammation and tumorigenesis by enhancing IL-6 and TNF expression. Cell 2010, 140: 197-208. 10.1016/j.cell.2009.12.052PubMedCentralCrossRefPubMed
8.
go back to reference Coaquette A, Bourgeois A, Dirand C, Varin A, Chen W, Herbein G: Mixed cytomegalovirus glycoprotein B genotypes in immunocompromised patients. Clin Infect Dis 2004, 39: 155-161. 10.1086/421496CrossRefPubMed Coaquette A, Bourgeois A, Dirand C, Varin A, Chen W, Herbein G: Mixed cytomegalovirus glycoprotein B genotypes in immunocompromised patients. Clin Infect Dis 2004, 39: 155-161. 10.1086/421496CrossRefPubMed
9.
go back to reference Khan KA, Coaquette A, Davrinche C, Herbein G: Bcl-3-regulated transcription from major immediate-early promoter of human cytomegalovirus in monocyte-derived macrophages. J Immunol 2009, 182: 7784-7794. 10.4049/jimmunol.0803800CrossRefPubMed Khan KA, Coaquette A, Davrinche C, Herbein G: Bcl-3-regulated transcription from major immediate-early promoter of human cytomegalovirus in monocyte-derived macrophages. J Immunol 2009, 182: 7784-7794. 10.4049/jimmunol.0803800CrossRefPubMed
10.
go back to reference Sinzger C, Digel M, Jahn G: Cytomegalovirus cell tropism. Curr Top Microbiol Immunol 2008, 325: 63-83. 10.1007/978-3-540-77349-8_4PubMed Sinzger C, Digel M, Jahn G: Cytomegalovirus cell tropism. Curr Top Microbiol Immunol 2008, 325: 63-83. 10.1007/978-3-540-77349-8_4PubMed
11.
go back to reference Michelson S: Interaction of human cytomegalovirus with monocytes/macrophages: a love-hate relationship. Pathol Biol (Paris) 1997, 45: 146-158. Michelson S: Interaction of human cytomegalovirus with monocytes/macrophages: a love-hate relationship. Pathol Biol (Paris) 1997, 45: 146-158.
12.
go back to reference Humbert M, Delattre RM, Fattal S, Rain B, Cerrina J, Dartevelle P, Simonneau G, Duroux P, Galanaud P, Emilie D: In situ production of interleukin-6 within human lung allografts displaying rejection or cytomegalovirus pneumonia. Transplantation 1993, 56: 623-627. 10.1097/00007890-199309000-00024CrossRefPubMed Humbert M, Delattre RM, Fattal S, Rain B, Cerrina J, Dartevelle P, Simonneau G, Duroux P, Galanaud P, Emilie D: In situ production of interleukin-6 within human lung allografts displaying rejection or cytomegalovirus pneumonia. Transplantation 1993, 56: 623-627. 10.1097/00007890-199309000-00024CrossRefPubMed
13.
go back to reference Humar A, St Louis P, Mazzulli T, McGeer A, Lipton J, Messner H, MacDonald KS: Elevated serum cytokines are associated with cytomegalovirus infection and disease in bone marrow transplant recipients. J Infect Dis 1999, 179: 484-488. 10.1086/314602CrossRefPubMed Humar A, St Louis P, Mazzulli T, McGeer A, Lipton J, Messner H, MacDonald KS: Elevated serum cytokines are associated with cytomegalovirus infection and disease in bone marrow transplant recipients. J Infect Dis 1999, 179: 484-488. 10.1086/314602CrossRefPubMed
14.
go back to reference Browne EP, Wing B, Coleman D, Shenk T: Altered cellular mRNA levels in human cytomegalovirus-infected fibroblasts: viral block to the accumulation of antiviral mRNAs. J Virol 2001, 75: 12319-12330. 10.1128/JVI.75.24.12319-12330.2001PubMedCentralCrossRefPubMed Browne EP, Wing B, Coleman D, Shenk T: Altered cellular mRNA levels in human cytomegalovirus-infected fibroblasts: viral block to the accumulation of antiviral mRNAs. J Virol 2001, 75: 12319-12330. 10.1128/JVI.75.24.12319-12330.2001PubMedCentralCrossRefPubMed
15.
go back to reference Carlquist JF, Edelman L, Bennion DW, Anderson JL: Cytomegalovirus induction of interleukin-6 in lung fibroblasts occurs independently of active infection and involves a G protein and the transcription factor, NF-kappaB. J Infect Dis 1999, 179: 1094-1100. 10.1086/314734CrossRefPubMed Carlquist JF, Edelman L, Bennion DW, Anderson JL: Cytomegalovirus induction of interleukin-6 in lung fibroblasts occurs independently of active infection and involves a G protein and the transcription factor, NF-kappaB. J Infect Dis 1999, 179: 1094-1100. 10.1086/314734CrossRefPubMed
16.
go back to reference Geist LJ, Dai LY: Cytomegalovirus modulates interleukin-6 gene expression. Transplantation 1996, 62: 653-658. 10.1097/00007890-199609150-00020CrossRefPubMed Geist LJ, Dai LY: Cytomegalovirus modulates interleukin-6 gene expression. Transplantation 1996, 62: 653-658. 10.1097/00007890-199609150-00020CrossRefPubMed
17.
go back to reference Chan G, Bivins-Smith ER, Smith MS, Smith PM, Yurochko AD: Transcriptome analysis reveals human cytomegalovirus reprograms monocyte differentiation toward an M1 macrophage. J Immunol 2008, 181: 698-711.PubMedCentralCrossRefPubMed Chan G, Bivins-Smith ER, Smith MS, Smith PM, Yurochko AD: Transcriptome analysis reveals human cytomegalovirus reprograms monocyte differentiation toward an M1 macrophage. J Immunol 2008, 181: 698-711.PubMedCentralCrossRefPubMed
18.
go back to reference Compton T, Kurt-Jones EA, Boehme KW, Belko J, Latz E, Golenbock DT, Finberg RW: Human cytomegalovirus activates inflammatory cytokine responses via CD14 and Toll-like receptor 2. J Virol 2003, 77: 4588-4596. 10.1128/JVI.77.8.4588-4596.2003PubMedCentralCrossRefPubMed Compton T, Kurt-Jones EA, Boehme KW, Belko J, Latz E, Golenbock DT, Finberg RW: Human cytomegalovirus activates inflammatory cytokine responses via CD14 and Toll-like receptor 2. J Virol 2003, 77: 4588-4596. 10.1128/JVI.77.8.4588-4596.2003PubMedCentralCrossRefPubMed
19.
go back to reference Fortunato EA, McElroy AK, Sanchez I, Spector DH: Exploitation of cellular signaling and regulatory pathways by human cytomegalovirus. Trends Microbiol 2000, 8: 111-119. 10.1016/S0966-842X(00)01699-1CrossRefPubMed Fortunato EA, McElroy AK, Sanchez I, Spector DH: Exploitation of cellular signaling and regulatory pathways by human cytomegalovirus. Trends Microbiol 2000, 8: 111-119. 10.1016/S0966-842X(00)01699-1CrossRefPubMed
20.
go back to reference Craig R, Larkin A, Mingo AM, Thuerauf DJ, Andrews C, McDonough PM, Glembotski CC: p38 MAPK and NF-kappa B collaborate to induce interleukin-6 gene expression and release. Evidence for a cytoprotective autocrine signaling pathway in a cardiac myocyte model system. J Biol Chem 2000, 275: 23814-23824. 10.1074/jbc.M909695199CrossRefPubMed Craig R, Larkin A, Mingo AM, Thuerauf DJ, Andrews C, McDonough PM, Glembotski CC: p38 MAPK and NF-kappa B collaborate to induce interleukin-6 gene expression and release. Evidence for a cytoprotective autocrine signaling pathway in a cardiac myocyte model system. J Biol Chem 2000, 275: 23814-23824. 10.1074/jbc.M909695199CrossRefPubMed
21.
go back to reference Ben-Neriah Y, Karin M: Inflammation meets cancer, with NF-kappaB as the matchmaker. Nat Immunol 2011, 12: 715-723.CrossRefPubMed Ben-Neriah Y, Karin M: Inflammation meets cancer, with NF-kappaB as the matchmaker. Nat Immunol 2011, 12: 715-723.CrossRefPubMed
22.
go back to reference Britt W: Manifestations of human cytomegalovirus infection: proposed mechanisms of acute and chronic disease. Curr Top Microbiol Immunol 2008, 325: 417-470. 10.1007/978-3-540-77349-8_23PubMed Britt W: Manifestations of human cytomegalovirus infection: proposed mechanisms of acute and chronic disease. Curr Top Microbiol Immunol 2008, 325: 417-470. 10.1007/978-3-540-77349-8_23PubMed
23.
go back to reference Staras SA, Dollard SC, Radford KW, Flanders WD, Pass RF, Cannon MJ: Seroprevalence of cytomegalovirus infection in the United States, 1988-1994. Clin Infect Dis 2006, 43: 1143-1151. 10.1086/508173CrossRefPubMed Staras SA, Dollard SC, Radford KW, Flanders WD, Pass RF, Cannon MJ: Seroprevalence of cytomegalovirus infection in the United States, 1988-1994. Clin Infect Dis 2006, 43: 1143-1151. 10.1086/508173CrossRefPubMed
24.
go back to reference Smieja M, Gnarpe J, Lonn E, Gnarpe H, Olsson G, Yi Q, Dzavik V, McQueen M, Yusuf S: Multiple infections and subsequent cardiovascular events in the Heart Outcomes Prevention Evaluation (HOPE) Study. Circulation 2003, 107: 251-257. 10.1161/01.CIR.0000044940.65226.1FCrossRefPubMed Smieja M, Gnarpe J, Lonn E, Gnarpe H, Olsson G, Yi Q, Dzavik V, McQueen M, Yusuf S: Multiple infections and subsequent cardiovascular events in the Heart Outcomes Prevention Evaluation (HOPE) Study. Circulation 2003, 107: 251-257. 10.1161/01.CIR.0000044940.65226.1FCrossRefPubMed
25.
go back to reference Aiello AE, Haan M, Blythe L, Moore K, Gonzalez JM, Jagust W: The influence of latent viral infection on rate of cognitive decline over 4 years. J Am Geriatr Soc 2006, 54: 1046-1054. 10.1111/j.1532-5415.2006.00796.xCrossRefPubMed Aiello AE, Haan M, Blythe L, Moore K, Gonzalez JM, Jagust W: The influence of latent viral infection on rate of cognitive decline over 4 years. J Am Geriatr Soc 2006, 54: 1046-1054. 10.1111/j.1532-5415.2006.00796.xCrossRefPubMed
26.
go back to reference Wang GC, Kao WH, Murakami P, Xue QL, Chiou RB, Detrick B, McDyer JF, Semba RD, Casolaro V, Walston JD, Fried LP: Cytomegalovirus infection and the risk of mortality and frailty in older women: a prospective observational cohort study. Am J Epidemiol 2010, 171: 1144-1152. 10.1093/aje/kwq062PubMedCentralCrossRefPubMed Wang GC, Kao WH, Murakami P, Xue QL, Chiou RB, Detrick B, McDyer JF, Semba RD, Casolaro V, Walston JD, Fried LP: Cytomegalovirus infection and the risk of mortality and frailty in older women: a prospective observational cohort study. Am J Epidemiol 2010, 171: 1144-1152. 10.1093/aje/kwq062PubMedCentralCrossRefPubMed
27.
28.
go back to reference Ten Napel HH, Houthoff HJ, The TH: Cytomegalovirus hepatitis in normal and immune compromised hosts. Liver 1984, 4: 184-194.CrossRefPubMed Ten Napel HH, Houthoff HJ, The TH: Cytomegalovirus hepatitis in normal and immune compromised hosts. Liver 1984, 4: 184-194.CrossRefPubMed
29.
go back to reference Soderberg-Naucler C: Does cytomegalovirus play a causative role in the development of various inflammatory diseases and cancer? J Intern Med 2006, 259: 219-246. 10.1111/j.1365-2796.2006.01618.xCrossRefPubMed Soderberg-Naucler C: Does cytomegalovirus play a causative role in the development of various inflammatory diseases and cancer? J Intern Med 2006, 259: 219-246. 10.1111/j.1365-2796.2006.01618.xCrossRefPubMed
30.
go back to reference Soderberg-Naucler C: HCMV microinfections in inflammatory diseases and cancer. J Clin Virol 2008, 41: 218-223. 10.1016/j.jcv.2007.11.009CrossRefPubMed Soderberg-Naucler C: HCMV microinfections in inflammatory diseases and cancer. J Clin Virol 2008, 41: 218-223. 10.1016/j.jcv.2007.11.009CrossRefPubMed
31.
go back to reference Cinatl J, Cinatl J, Vogel JU, Rabenau H, Kornhuber B, Doerr HW: Modulatory effects of human cytomegalovirus infection on malignant properties of cancer cells. Intervirology 1996, 39: 259-269.PubMed Cinatl J, Cinatl J, Vogel JU, Rabenau H, Kornhuber B, Doerr HW: Modulatory effects of human cytomegalovirus infection on malignant properties of cancer cells. Intervirology 1996, 39: 259-269.PubMed
32.
go back to reference Bain M, Sinclair J: The S phase of the cell cycle and its perturbation by human cytomegalovirus. Rev Med Virol 2007, 17: 423-434. 10.1002/rmv.551CrossRefPubMed Bain M, Sinclair J: The S phase of the cell cycle and its perturbation by human cytomegalovirus. Rev Med Virol 2007, 17: 423-434. 10.1002/rmv.551CrossRefPubMed
34.
go back to reference Cobbs CS, Harkins L, Samanta M, Gillespie GY, Bharara S, King PH, Nabors LB, Cobbs CG, Britt WJ: Human cytomegalovirus infection and expression in human malignant glioma. Cancer Res 2002, 62: 3347-3350.PubMed Cobbs CS, Harkins L, Samanta M, Gillespie GY, Bharara S, King PH, Nabors LB, Cobbs CG, Britt WJ: Human cytomegalovirus infection and expression in human malignant glioma. Cancer Res 2002, 62: 3347-3350.PubMed
35.
go back to reference Harkins L, Volk AL, Samanta M, Mikolaenko I, Britt WJ, Bland KI, Cobbs CS: Specific localisation of human cytomegalovirus nucleic acids and proteins in human colorectal cancer. Lancet 2002, 360: 1557-1563. 10.1016/S0140-6736(02)11524-8CrossRefPubMed Harkins L, Volk AL, Samanta M, Mikolaenko I, Britt WJ, Bland KI, Cobbs CS: Specific localisation of human cytomegalovirus nucleic acids and proteins in human colorectal cancer. Lancet 2002, 360: 1557-1563. 10.1016/S0140-6736(02)11524-8CrossRefPubMed
36.
go back to reference Samanta M, Harkins L, Klemm K, Britt WJ, Cobbs CS: High prevalence of human cytomegalovirus in prostatic intraepithelial neoplasia and prostatic carcinoma. J Urol 2003, 170: 998-1002. 10.1097/01.ju.0000080263.46164.97CrossRefPubMed Samanta M, Harkins L, Klemm K, Britt WJ, Cobbs CS: High prevalence of human cytomegalovirus in prostatic intraepithelial neoplasia and prostatic carcinoma. J Urol 2003, 170: 998-1002. 10.1097/01.ju.0000080263.46164.97CrossRefPubMed
37.
go back to reference Zafiropoulos A, Tsentelierou E, Billiri K, Spandidos DA: Human herpes viruses in non-melanoma skin cancers. Cancer Lett 2003, 198: 77-81. 10.1016/S0304-3835(03)00269-6CrossRefPubMed Zafiropoulos A, Tsentelierou E, Billiri K, Spandidos DA: Human herpes viruses in non-melanoma skin cancers. Cancer Lett 2003, 198: 77-81. 10.1016/S0304-3835(03)00269-6CrossRefPubMed
38.
go back to reference Guetta E, Guetta V, Shibutani T, Epstein SE: Monocytes harboring cytomegalovirus: interactions with endothelial cells, smooth muscle cells, and oxidized low-density lipoprotein. Possible mechanisms for activating virus delivered by monocytes to sites of vascular injury. Circ Res 1997, 81: 8-16.CrossRefPubMed Guetta E, Guetta V, Shibutani T, Epstein SE: Monocytes harboring cytomegalovirus: interactions with endothelial cells, smooth muscle cells, and oxidized low-density lipoprotein. Possible mechanisms for activating virus delivered by monocytes to sites of vascular injury. Circ Res 1997, 81: 8-16.CrossRefPubMed
39.
go back to reference Porta C, De Amici M, Quaglini S, Paglino C, Tagliani F, Boncimino A, Moratti R, Corazza GR: Circulating interleukin-6 as a tumor marker for hepatocellular carcinoma. Ann Oncol 2008, 19: 353-358. 10.1093/annonc/mdm448CrossRefPubMed Porta C, De Amici M, Quaglini S, Paglino C, Tagliani F, Boncimino A, Moratti R, Corazza GR: Circulating interleukin-6 as a tumor marker for hepatocellular carcinoma. Ann Oncol 2008, 19: 353-358. 10.1093/annonc/mdm448CrossRefPubMed
40.
go back to reference Cheng KS, Tang HL, Chou FT, Chou JW, Hsu CH, Yu CJ, Kao ST, Li TC: Cytokine evaluation in liver cirrhosis and hepatocellular carcinoma. Hepatogastroenterology 2009, 56: 1105-1110.PubMed Cheng KS, Tang HL, Chou FT, Chou JW, Hsu CH, Yu CJ, Kao ST, Li TC: Cytokine evaluation in liver cirrhosis and hepatocellular carcinoma. Hepatogastroenterology 2009, 56: 1105-1110.PubMed
41.
go back to reference Wiest R, Weigert J, Wanninger J, Neumeier M, Bauer S, Schmidhofer S, Farkas S, Scherer MN, Schaffler A, Scholmerich J, Buechler C: Impaired hepatic removal of interleukin-6 in patients with liver cirrhosis. Cytokine 2011, 53: 178-183. 10.1016/j.cyto.2010.06.013CrossRefPubMed Wiest R, Weigert J, Wanninger J, Neumeier M, Bauer S, Schmidhofer S, Farkas S, Scherer MN, Schaffler A, Scholmerich J, Buechler C: Impaired hepatic removal of interleukin-6 in patients with liver cirrhosis. Cytokine 2011, 53: 178-183. 10.1016/j.cyto.2010.06.013CrossRefPubMed
42.
go back to reference Poynard T, Yuen MF, Ratziu V, Lai CL: Viral hepatitis C. Lancet 2003, 362: 2095-2100. 10.1016/S0140-6736(03)15109-4CrossRefPubMed Poynard T, Yuen MF, Ratziu V, Lai CL: Viral hepatitis C. Lancet 2003, 362: 2095-2100. 10.1016/S0140-6736(03)15109-4CrossRefPubMed
43.
go back to reference Falleti E, Fabris C, Vandelli C, Colletta C, Cussigh A, Smirne C, Fontanini E, Cmet S, Minisini R, Bitetto D, et al.: Genetic polymorphisms of interleukin-6 modulate fibrosis progression in mild chronic hepatitis C. Hum Immunol 2010, 71: 999-1004. 10.1016/j.humimm.2010.06.006CrossRefPubMed Falleti E, Fabris C, Vandelli C, Colletta C, Cussigh A, Smirne C, Fontanini E, Cmet S, Minisini R, Bitetto D, et al.: Genetic polymorphisms of interleukin-6 modulate fibrosis progression in mild chronic hepatitis C. Hum Immunol 2010, 71: 999-1004. 10.1016/j.humimm.2010.06.006CrossRefPubMed
44.
go back to reference Giannitrapani L, Soresi M, Giacalone A, Campagna ME, Marasa M, Cervello M, Marasa S, Montalto G: IL-6 -174G/C polymorphism and IL-6 serum levels in patients with liver cirrhosis and hepatocellular carcinoma. Omics 2011, 15: 183-186. 10.1089/omi.2010.0093CrossRefPubMed Giannitrapani L, Soresi M, Giacalone A, Campagna ME, Marasa M, Cervello M, Marasa S, Montalto G: IL-6 -174G/C polymorphism and IL-6 serum levels in patients with liver cirrhosis and hepatocellular carcinoma. Omics 2011, 15: 183-186. 10.1089/omi.2010.0093CrossRefPubMed
45.
go back to reference Cussigh A, Falleti E, Fabris C, Bitetto D, Cmet S, Fontanini E, Bignulin S, Fornasiere E, Fumolo E, Minisini R, et al.: Interleukin 6 promoter polymorphisms influence the outcome of chronic hepatitis C. Immunogenetics 2011, 63: 33-41. 10.1007/s00251-010-0491-7CrossRefPubMed Cussigh A, Falleti E, Fabris C, Bitetto D, Cmet S, Fontanini E, Bignulin S, Fornasiere E, Fumolo E, Minisini R, et al.: Interleukin 6 promoter polymorphisms influence the outcome of chronic hepatitis C. Immunogenetics 2011, 63: 33-41. 10.1007/s00251-010-0491-7CrossRefPubMed
46.
go back to reference Dendorfer U, Oettgen P, Libermann TA: Multiple regulatory elements in the interleukin-6 gene mediate induction by prostaglandins, cyclic AMP, and lipopolysaccharide. Mol Cell Biol 1994, 14: 4443-4454.PubMedCentralCrossRefPubMed Dendorfer U, Oettgen P, Libermann TA: Multiple regulatory elements in the interleukin-6 gene mediate induction by prostaglandins, cyclic AMP, and lipopolysaccharide. Mol Cell Biol 1994, 14: 4443-4454.PubMedCentralCrossRefPubMed
47.
go back to reference Trautwein C, Caelles C, van der Geer P, Hunter T, Karin M, Chojkier M: Transactivation by NF-IL6/LAP is enhanced by phosphorylation of its activation domain. Nature 1993, 364: 544-547. 10.1038/364544a0CrossRefPubMed Trautwein C, Caelles C, van der Geer P, Hunter T, Karin M, Chojkier M: Transactivation by NF-IL6/LAP is enhanced by phosphorylation of its activation domain. Nature 1993, 364: 544-547. 10.1038/364544a0CrossRefPubMed
48.
go back to reference Vanden Berghe W, Vermeulen L, De Wilde G, De Bosscher K, Boone E, Haegeman G: Signal transduction by tumor necrosis factor and gene regulation of the inflammatory cytokine interleukin-6. Biochem Pharmacol 2000, 60: 1185-1195. 10.1016/S0006-2952(00)00412-3CrossRefPubMed Vanden Berghe W, Vermeulen L, De Wilde G, De Bosscher K, Boone E, Haegeman G: Signal transduction by tumor necrosis factor and gene regulation of the inflammatory cytokine interleukin-6. Biochem Pharmacol 2000, 60: 1185-1195. 10.1016/S0006-2952(00)00412-3CrossRefPubMed
49.
go back to reference Naugler WE, Sakurai T, Kim S, Maeda S, Kim K, Elsharkawy AM, Karin M: Gender disparity in liver cancer due to sex differences in MyD88-dependent IL-6 production. Science 2007, 317: 121-124. 10.1126/science.1140485CrossRefPubMed Naugler WE, Sakurai T, Kim S, Maeda S, Kim K, Elsharkawy AM, Karin M: Gender disparity in liver cancer due to sex differences in MyD88-dependent IL-6 production. Science 2007, 317: 121-124. 10.1126/science.1140485CrossRefPubMed
50.
go back to reference Heinrich PC, Behrmann I, Haan S, Hermanns HM, Muller-Newen G, Schaper F: Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem J 2003, 374: 1-20. 10.1042/BJ20030407PubMedCentralCrossRefPubMed Heinrich PC, Behrmann I, Haan S, Hermanns HM, Muller-Newen G, Schaper F: Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem J 2003, 374: 1-20. 10.1042/BJ20030407PubMedCentralCrossRefPubMed
51.
go back to reference Ghoreschi K, Laurence A, O'Shea JJ: Selectivity and therapeutic inhibition of kinases: to be or not to be? Nat Immunol 2009, 10: 356-360. 10.1038/ni.1701PubMedCentralCrossRefPubMed Ghoreschi K, Laurence A, O'Shea JJ: Selectivity and therapeutic inhibition of kinases: to be or not to be? Nat Immunol 2009, 10: 356-360. 10.1038/ni.1701PubMedCentralCrossRefPubMed
52.
go back to reference Taub R: Liver regeneration 4: transcriptional control of liver regeneration. Faseb J 1996, 10: 413-427.PubMed Taub R: Liver regeneration 4: transcriptional control of liver regeneration. Faseb J 1996, 10: 413-427.PubMed
53.
go back to reference Lassoued W, Murphy D, Tsai J, Oueslati R, Thurston G, Lee WM: Effect of VEGF and VEGF Trap on vascular endothelial cell signaling in tumors. Cancer Biol Ther 2011, 10: 1326-1333.CrossRef Lassoued W, Murphy D, Tsai J, Oueslati R, Thurston G, Lee WM: Effect of VEGF and VEGF Trap on vascular endothelial cell signaling in tumors. Cancer Biol Ther 2011, 10: 1326-1333.CrossRef
54.
go back to reference Calvisi DF, Ladu S, Gorden A, Farina M, Conner EA, Lee JS, Factor VM, Thorgeirsson SS: Ubiquitous activation of Ras and Jak/Stat pathways in human HCC. Gastroenterology 2006, 130: 1117-1128. 10.1053/j.gastro.2006.01.006CrossRefPubMed Calvisi DF, Ladu S, Gorden A, Farina M, Conner EA, Lee JS, Factor VM, Thorgeirsson SS: Ubiquitous activation of Ras and Jak/Stat pathways in human HCC. Gastroenterology 2006, 130: 1117-1128. 10.1053/j.gastro.2006.01.006CrossRefPubMed
55.
go back to reference Chen RH, Chang MC, Su YH, Tsai YT, Kuo ML: Interleukin-6 inhibits transforming growth factor-beta-induced apoptosis through the phosphatidylinositol 3-kinase/Akt and signal transducers and activators of transcription 3 pathways. J Biol Chem 1999, 274: 23013-23019. 10.1074/jbc.274.33.23013CrossRefPubMed Chen RH, Chang MC, Su YH, Tsai YT, Kuo ML: Interleukin-6 inhibits transforming growth factor-beta-induced apoptosis through the phosphatidylinositol 3-kinase/Akt and signal transducers and activators of transcription 3 pathways. J Biol Chem 1999, 274: 23013-23019. 10.1074/jbc.274.33.23013CrossRefPubMed
56.
go back to reference Cheeran MC, Mutnal MB, Hu S, Armien A, Lokensgard JR: Reduced lymphocyte infiltration during cytomegalovirus brain infection of interleukin-10-deficient mice. J Neurovirol 2009, 15: 334-342. 10.1080/13550280903062797PubMedCentralCrossRefPubMed Cheeran MC, Mutnal MB, Hu S, Armien A, Lokensgard JR: Reduced lymphocyte infiltration during cytomegalovirus brain infection of interleukin-10-deficient mice. J Neurovirol 2009, 15: 334-342. 10.1080/13550280903062797PubMedCentralCrossRefPubMed
57.
58.
59.
go back to reference Quach N, Goodman MF, Shibata D: In vitro mutation artifacts after formalin fixation and error prone translesion synthesis during PCR. BMC Clin Pathol 2004, 4: 1. 10.1186/1472-6890-4-1PubMedCentralCrossRefPubMed Quach N, Goodman MF, Shibata D: In vitro mutation artifacts after formalin fixation and error prone translesion synthesis during PCR. BMC Clin Pathol 2004, 4: 1. 10.1186/1472-6890-4-1PubMedCentralCrossRefPubMed
60.
go back to reference Pass RF, Zhang C, Evans A, Simpson T, Andrews W, Huang ML, Corey L, Hill J, Davis E, Flanigan C, Cloud G: Vaccine prevention of maternal cytomegalovirus infection. N Engl J Med 2009, 360: 1191-1199. 10.1056/NEJMoa0804749PubMedCentralCrossRefPubMed Pass RF, Zhang C, Evans A, Simpson T, Andrews W, Huang ML, Corey L, Hill J, Davis E, Flanigan C, Cloud G: Vaccine prevention of maternal cytomegalovirus infection. N Engl J Med 2009, 360: 1191-1199. 10.1056/NEJMoa0804749PubMedCentralCrossRefPubMed
61.
go back to reference Colugnati FA, Staras SA, Dollard SC, Cannon MJ: Incidence of cytomegalovirus infection among the general population and pregnant women in the United States. BMC Infect Dis 2007, 7: 71. 10.1186/1471-2334-7-71PubMedCentralCrossRefPubMed Colugnati FA, Staras SA, Dollard SC, Cannon MJ: Incidence of cytomegalovirus infection among the general population and pregnant women in the United States. BMC Infect Dis 2007, 7: 71. 10.1186/1471-2334-7-71PubMedCentralCrossRefPubMed
Metadata
Title
Increased HCMV seroprevalence in patients with hepatocellular carcinoma
Authors
Quentin Lepiller
Manoj K Tripathy
Vincent Di Martino
Bernadette Kantelip
Georges Herbein
Publication date
01-12-2011
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2011
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/1743-422X-8-485

Other articles of this Issue 1/2011

Virology Journal 1/2011 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.