Underlying pathophysiology of HCV infection in HIV-positive drug users

Journal of Addictive Diseases

Volumn 27, Issue 2, 2008, Pages 75-82

  Balasubramanian, Anuradha ^a   Groopman, Jerome E ^a   Ganju, Ramesh K ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD INSTITUTES OF MEDICINE   (United States)

Author keywords

Cell death; Drug user; HCV; HIV; Inflammation

Indexed keywords

APOPTOSIS; CELL DEATH; CYTOKINE PRODUCTION; DISEASE COURSE; DRUG DEPENDENCE; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IN VIVO STUDY; LIVER CELL; LIVER CIRRHOSIS; LIVER DISEASE; MIXED INFECTION; PATHOGENESIS; PATHOPHYSIOLOGY; REVIEW; RISK FACTOR; IMMUNOLOGY; INFLAMMATION; PATHOLOGY; SUBSTANCE ABUSE;

CD4 ANTIGEN; CD8 ANTIGEN;

ANTIGENS, CD4; ANTIGENS, CD8; CELL DEATH; DISEASE PROGRESSION; HEPATITIS C, CHRONIC; HIV INFECTIONS; HUMANS; INFLAMMATION; LIVER CIRRHOSIS; SUBSTANCE ABUSE, INTRAVENOUS;

EID: 52049088300     PISSN: 10550887     EISSN: 15450848     Source Type: Journal    
DOI: 10.1300/J069v27n02_09     Document Type: Review

References (84)

1. Houghton M. Hepatitis C virus. In: Fields BN, Knipe DM, Howley PM, (eds.), Fields Virology. Philadelphia: Lippincott-Raven, 1996:1035-1058.
2. Hoofnagle JH. Course and outcome of hepatitis C. Hepatology. 2002; 36:S21-S29.
3. Lindenbach BD, Rice CM. Flaviviridae: The viruses and their replication. In: Knipe DM, Howley PM, (eds.), Fields Virology. Philadelphia: Lippincott-Raven, 2001:991-1041.
4. Deforges S, Evlashev A, Perret M, Sodoyer M, Pouzel S, Scoazec JY, Bonnaud B, Diaz O, Paranhos-Baccala G, Lotteau V, Andre P. Expression of hepatitis C virus proteins in epithelial intestinal cells in vivo. J Gen Virol. 2004; 85:2515-2523.
5. 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.
6. Bowen DG, Walker CM. The origin of quasispecies: cause or consequence of chronic hepatitis C viral infection? J Hepatol. 2005; 42:408-417.
7. Neumann AU, Lam NP, Dahari H, Gretch DR, Wiley TE, Layden TJ, Perelson AS. Hepatitis C viral dynamics in vivo and the antiviral efficacy of interferon-alpha therapy. Science. 1998; 282:103-107.
8. Alter MJ. Epidemiology of hepatitis C. Eur J Gastroenterol Hepatol. 1996; 8:319-323.
9. Alter MJ. Epidemiology of hepatitis C. Hepatology. 1997; 26:62S-65S.
10. Alter MJ. Hepatitis C virus infection in the United States. J Hepatol. 1999; 20:731-735.
11. Alter MJ. Prevention of spread of hepatitis C. Hepatology. 2002; 36:S93-S98.
12. Dore GJ, Thomas DL. Management and treatment of injection drug users with hepatitis C virus (HCV) infection and HCV/human immunodeficiency virus co-infection. Semin Liver Dis. 2005; 25:18-32.
13. Crofts N, Aitken CK. Incidence of blood borne virus infection and risk behaviors in a cohort of injecting drug users in Victoria, 1990-1995. Med J Aust. 1997; 167:17-20.
14. Hahn JA, Page-Shafer K, Lum PJ, Bourgois P, Stein E, Evans JL, Busch MP, Tobler LH, Phelps B, Moss AR. Hepatitis C virus seroconversion among young injection drug users: relationships and risks. J Infect Dis. 2002; 186:1558-1564.
15. Ostapowicz G, Watson KJ, Locarnini SA, Desmond PV. Role of alcohol in the progression of liver disease caused by hepatitis C virus infection. Hepatology. 1998; 27:1730-1735.
16. McCance-Katz EF. Treatment of opioid dependence and coinfection with HIV and hepatitis C virus in opioid-dependent patients: the importance of drug interactions between opioids and antiretroviral agents. Clin Infect Dis. 2005; 41:S89-S95.
17. Kumar GN, Rodrigues AD, Buko AM, Denissen JF. Cytochrome P450-mediated metabolism of the HIV-1 protease inhibitor ritonavir (ABT-538) in human liver microsomes. J Pharmacol Exp Ther. 1996; 277:423-431.
18. Thomas DL. Hepatitis C and human immunodeficiency virus infection. Hepatology. 2002; 36:S201-209.
19. Sulkowski MS, Thomas DL. Hepatitis C in the HIV-infected person. Ann Intern Med. 2003; 138:197-207.
20. Sulkowski MS, Mast EE, Seeff LB, Thomas DL. Hepatitis C virus infection as an opportunistic disease in persons infected with human immunodeficiency virus. Clin Infect Dis. 2000; 30:S77-S84.
21. Proceedings of the International Workshop on Epidemiology. Diagnosis and management of hepatitis C infection. Medicine and the Community. 1996; 6-7: 1-32.
22. Sharara AI, Hunt CM, Hamilton JD. Hepatitis C. Ann Intern Med. 1996; 125:658-668.
23. Di Bisceglie AM. Hepatitis C. Lancet. 1998; 351:351-355.
24. Fingerhood MI, Jasinski DR, Sullivan JT. Prevalence of hepatitis C in a chemically dependent population. Arch Intern Med. 1993; 153:2025-2030.
25. Persico M, Romano M. Alanine aminotransferase measurements and histological disease in hepatitis C. Lancet 1993; 342:1369-1370.
26. Tong MJ, el-Farra NS. Clinical sequelae of hepatitis C acquired from injection drug use. West J Med. 1996; 164:399-404.
27. Tennant F. Hepatitis C, B, D, and A: contrasting features and liver function abnormalities in heroin addicts. J Addict Dis. 2001; 20:9-17.
28. Moss RA, Okun DB. Heroin-induced thrombocytopenia. Arch Intern Med. 1979; 139:752-754.
29. Tennant F, Moll D. Seroprevalence of hepatitis A, B, C, and D markers and liver function abnormalities in intravenous heroin addicts. J Addict Dis. 1995; 14: 35-49.
30. Smith CS, Paauw DS. Hepatocellular carcinoma. Identifying and screening populations at increased risk. Postgrad Med. 1993; 98:71-74.
31. EASL International Consensus conference on Hepatitis C. Consensus statement. J Hepatol. 1999; 31: 3-8.
32. Garcia-Samaniego J, Rodriguez M, Berenguer J, Rodriguez-Rosado R, Carbo J, Asensi V, Soriano V. Hepatocellular carcinoma in HIV-infected patients with chronic hepatitis C. Am J Gastroenterol. 2001; 96:179-183.
33. Graham CS, Baden LR, Yu E, Mrus JM, Carnie J, Heeren T, Koziel MJ. Influence of human immunodeficiency virus infection on the course of hepatitis C virus infection: a meta-analysis. Clin Infect Dis. 2001; 33: 562-569.
34. Monga HK, Rodriguez-Barradas MC, Breaux K, Khattak K, Troisi CL, Velez M, Yoffe B. Hepatitis C virus infection-related morbidity and mortality among patients with human immunodeficiency virus infection. Clin Infect Dis. 2001; 33:240-247.
35. Hisada M, Chatterjee N, Kalaylioglu Z, Battjes RJ, Goedert JJ. Hepatitis C virus load and survival among injection drug users in the United States. Hepatology. 2005; 42:1446-1452.
36. Strader DB. Coinfection with HIV and hepatitis C virus in injection drug users and minority populations. Clin Infect Dis. 2005; 41:S7-S13.
37. Garten RJ, Zhang J, Lai S, Liu W, Chen J, Yu XF. Coinfection with HIV and hepatitis C virus among injection drug users in southern China. Clin Infect Dis. 2005; 41:S18-S24.
38. Khalsa JH, Kresina T, Sherman K, Vocci F. Medical management of HIV-hepatitis C virus coinfection in injection drug users. Clin Infect Dis. 2005; 41:S1-S6.
39. Koziel MJ, Cellular immune responses against hepatitis C virus. Clin Infect Dis. 2005; 41:S25-S31.
40. Greub G, Ledergerber B, Battegay M, Grob P, Perrin L, Furrer H, Burgisser P, Erb P, Boggian K, Piffaretti JC, Hirschel B, Janin P, Francioli P, Flepp M, Telenti A. Clinical progression, survival, and immune recovery during antiretroviral therapy in patients with HIV-1 and hepatitis C virus coinfection: the Swiss HIV Cohort Study. Lancet. 2000; 356:1800-1805.
41. Hilsabeck RC, Castellon SA, Hinkin CH. Neuropsychological aspects of coinfection with HIV and hepatitis C virus. Clin Infect Dis. 2005; 41:S38-S44.
42. Gonzalez R, JacobusJ, Martin EM. Investigating neurocognitive features of hepatitis C virus infection in drug users: potential challenges and lessons learned from the HIV literature. Clin Infect Dis. 2005; 41: S45-S49.
43. Neff GW, Shire NJ, Rudich SM. Outcomes among patients with end-stage liver disease who are coinfected with HIV and hepatitis C virus. Clin Infect Dis. 2005; 41:S50-S55.
44. Soriano V, Garcia-Samaniego J, Valencia E, Rodriguez-Rosado R, Munoz F, Gonzalez-Lahoz J. Impact of chronic liver disease due to hepatitis viruses as cause of hospital admission and death in HIV-infected drug users. Eur J Epidemiol. 1999; 15:1-4.
45. Choo QL, Kuo G, Weiner AJ, Overby LR, Bradley DW, Houghton M. Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science. 1989; 244:359-362.
46. Kaplanski G, Farnarier C, Payan MJ, Bongrand P, Durand JM. Increased levels of soluble adhesion molecules in the serum of patients with hepatitis C. Correlation with cytokine concentrations and liver inflammation and fibrosis. Dig Dis Sci.1997; 42:2277-2284.
47. Masumoto T, Ohkubo K, Yamamoto K, Ninomiya T, Abe M, Akbar SM, Michitaka K, Horiike N, Onji M. Serum IL-8 levels and localization of IL-8 in liver from patients with chronic viral hepatitis. Hepatogastroenterology. 1998; 45:1630-1634.
48. Marie C, Losser MR, Fitting C, Kermarrec N, Payen D, Cavaillon JM. Cytokines and soluble cytokine receptors in pleural effusions from septic and nonseptic patients. Am J Respir Crit Care Med. 1997; 156: 1512-1522.
49. Marty C, Misset B, Tamion F, Fitting C, Carlet J, Cavaillon JM. Circulating interleukin-8 concentrations in patients with multiple organ failure of septic and nonseptic origin. Crit. Care Med. 1994; 22:673-679.
50. Dienes HP, Drebber U, vonBoth I. Liver biopsy in hepatitis C. J Hepatol. 1999; 31:43-46.
51. Iio S, Hayashi N, Mita E, Ueda K, Mochizuki, Hiramatsu N, Kanto T, Sasaki Y, Kasahara A, Hori M. Serum levels of soluble Fas antigen in chronic hepatitis C patients. J Hepatol. 1998; 29:517-523.
52. Daniel V, Sadeghi M, Naujokat C, Weimer R, Huth-Kuhne A, Zimmermann R, Opelz G. Evidence for autoantibody-induced CD4 depletion mediated by apoptotic and non-apoptotic mechanisms in HIV-positive long-term surviving haemophilia patients. Clin Exp Immunol. 2004; 135:94-104.
53. Castedo, M, Perfettini JL, Andreau K, Roumier T, Piacentini M, Kroemer G. Mitochondrial apoptosis induced by the HIV-1 envelope. Ann NY Acad Sci. 2003; 1010:9-28.
54. Macias J, Japon MA, Saez C, Palacios RB, Mira JA, Garcia-Garcia JA, Merchante N, Vergara S, Lozano F, Gomez-Mateos J, Pineda JA. Increased hepatocyte Fas expression and apoptosis in HIV and Hepatitis C virus coinfection. J Infect Dis. 2005; 192:1566-1576.
55. Baggiolini M.Chemokines and leukocyte traffic. Nature. 1998; 392:565-568.
56. Penna A, Missale G, Lamonaca V, Pilli M, Mori C, Zanelli P, Cavalli A, Elia G, Ferrari C. Intrahepatic and circulating HLA class II-restricted, hepatitis C virusspecific T cells: functional characterization in patients with chronic hepatitis C. Hepatology. 2002; 35:1225-1236.
57. Rico MA, Quiroga JA, Subira D, Garcia E, Castanon S, Sallberg M, Leroux-Roels G, Weiland O, Pardo M, Carreno V. Features of the CD4 + T-cell response in liver and peripheral blood of hepatitis C virusinfected patients with persistently normal and abnormal alanine aminotransferase levels. J Hepatol. 2002; 36: 408-416.
58. Benhamou Y, Bochet M, Di Martino V, Charlotte F, Azria F, Coutellier A, Vidaud M, Bricaire F, Opolon P, Katlama C, Poynard T. Liver fibrosis progression in human immunodeficiency virus and hepatitis C virus coinfected patients. The Multivirc Group. Hepatology. 1999; 30:1054-1058.
59. Valdez H, Anthony D, Farukhi F, Patki A, Salkowitz J, Heeger P, Peterson DL, Post AB, Asaad R, Lederman MM. Immune responses to hepatitis C and non-hepatitis C antigens in hepatitis C virus infected and HIV-1 coinfected patients. AIDS. 2000; 14:2239-2246.
60. Lauer GM, Nguyen TN, Day CL, Robbins GK, Flynn T, McGowan K, Rosenberg ES, Lucas M, Klenerman P, Chung RT, Walker BD. Human immunodeficiency virus type 1-hepatitis C virus coinfection: intraindividual comparison of cellular immune responses against two persistent viruses. J Virol. 2002; 76:2817-2826.
61. Kim AY, Lauer GM, Ouchi K,Addo MM, Lucas M, Wiesch JS, Timm J, Boczanowski M, Duncan JE, Wurcel AG, Casson D, Chung RT, Draenert R, Klenerman P, Walker BD. The magnitude and breadth of hepatitis C virus-specific CD8 + T cells depend on absolute CD4 + T-cell count in individuals coinfected with HIV-1. Blood. 2005; 105:1170-1178.
62. Okuda M, Li K, Beard MR, Showalter LA, Scholle F, Lemon SM, Weinman SA. Mitochondrial injury, oxidative stress, and antioxidant gene expression are induced by hepatitis C virus core protein. Gastroenterology. 2002; 122:366-375.
63. Zhao LJ, Wang L, Ren H, Cao J, Li L, Ke JS, Qi ZT. Hepatitis C virus E2 protein promotes human hepatoma cell proliferation through the MAPK/ERK signaling pathway via cellular receptors. Exp Cell Res. 2005; 305:23-32.
64. Feng DY, Sun Y, Cheng RX, Ouyang XM, Zheng H. Effect of hepatitis C virus nonstructural protein NS3 on proliferation and MAPK phosphorylation of normal hepatocyte line. World J Gastroenterol. 2005; 11:2157-2161.
65. Gong G, Waris G, Tanveer R, Siddiqui A. Human hepatitis C virus NS5A protein alters intracellular calcium levels, induces oxidative stress, and activates STAT-3 and NF-kappa B. Proc Natl Acad Sci USA. 2001; 98:9599-9604.
66. Lai MM. Hepatitis C virus proteins: direct link to hepatic oxidative stress, steatosis, carcinogenesis and more. Gastroenterology. 2002; 122:568-571.
67. Blackard JT, Komurian-Pradel F, Perret M, Sodoyer M, Smeaton L, Clair JB, Chapman S, Taylor LE, Paranhos-Baccala G, Chung RT. Intrahepatic cytokine expression is downregulated during HCV/HIV co-infection. J Med Virol. 2006; 78:202-207.
68. Hourigan LF, Macdonald GA, Purdie D, Whitehall VH, Shorthouse C, Clouston A, Powell EE. Fibrosis in chronic hepatitis C correlates significantly with body mass index and steatosis. Hepatology. 1999; 29:1215-1219.
69. Schneiderman DJ, Arenson DM, Cello JP, Margaretten W, Weber TE. Hepatic disease in patients with the acquired immune deficiency syndrome (AIDS). Hepatology. 1987; 7:925-930.
70. Sulkowski MS, Mehta SH, Toberson M, Afdhal NH, Mirel L, Moore RD, Thomas DL. Hepatic steatosis and antiretroviral drug use among adults coinfected with HIV and hepatitis C virus. AIDS. 2005; 19:585-592.
71. Monto A, Dove LM, Bostrom A, Kakar S, Tien PC, Wright TL. Hepatic steatosis in HIV/hepatitis C coinfection: prevalence and significance compared with hepatitis C monoinfection. Hepatology. 2005; 42:310-316.
72. Pol S, Fontaine H, Carnot F, Zylberberg H, Berthelot P, Brechot C, Nalpas B. Predictive factors for development of cirrhosis in parenterally acquired chronic hepatitis C: a comparison between immunocompetent and immunocompromised patients. J Hepatol. 1998; 29:12-19.
73. Mohsen AH, Easterbrook PJ, Taylor C, Portmann B, Kulasegaram R, Murad S, Wiselka M, Norris S. Impact of human immunodeficiency virus (HIV) infection on the progression of liver fibrosis in hepatitis C virus infected patients. Gut. 2003; 52:1035-1040.
74. Balasubramanian A, Ganju RK, Groopman JE. Hepatitis C virus and HIV envelope proteins collaboratively mediate interleukin-8 secretion through activation of p38 MAP kinase and SHP2 in hepatocytes. J Biol Chem. 2003; 278:35755-35766.
75. Munshi N, Balasubramanian A, Koziel M, Ganju RK, Groopman JE. Hepatitis C and human immunodeficiency virus envelope proteins cooperatively induce hepatocytic apoptosis via an innocent bystander mechanism. J Infect Dis. 2003; 188:1192-1204.
76. Balasubramanian A, Koziel MJ, Groopman JE, Ganju RK. Molecular mechanism of hepatic injury in coinfection with hepatitis C virus and HIV. Clin Infect Dis. 2005; 41:S32-S37.
77. Balasubramanian A, Ganju RK, Groopman JE. Stat1 mediates apoptosis induced by HCV and HIV envelope proteins in hepatocytes. J Infect Dis. 2006;194: 670-681.
78. Balasubramanian A, Munshi N, Koziel MJ, Hu Z, Liang TJ, Groopman JE, Ganju RK. Structural proteins of Hepatitis C virus induce interleukin 8 production and apoptosis in human endothelial cells. J Gen Virol. 2005; 86:3291-3301.
79. Spanakis NE, Garinis GA, Alexopoulos EC, Patrinos GP, Menounos PG, Sklavounou A, Manolis EN, Gorgoulis VG, Valis D. Cytokine serum levels in patients with chronic HCV infection. J Clin Lab Anal. 2002; 16:40-46.
80. Fukuda R, Ishimura N, Ishihara S, Chowdhury A, Morlyama N, Nogami C, Miyake T, Niigaki M, Tokuda A, Satoh S, Sakai S, Akagi S, Watanabe M, Fukumoto S. Intrahepatic expression of pro-inflammatory cytokine mRNAs and interferon efficacy in chronic hepatitis C. Liver, 1996; 16:390-399.
81. Polyak SJ, Khabar KS, Rezeiq M, Gretch DR. Elevated levels of interleukin-8 in serum are associated with hepatitis C virus infection and resistance to interferon therapy. J Virol. 2001; 75:6209-6211.
82. Gochee PA, Jonsson JR, Closton AD, Pandeya N, Purdie DM, Powell EE. Steatosis in chronic hepatitis C: association with increased messenger RNA expression of collagen I, tumor necrosis factor-alpha and cytochrome P450 2E1. J Gastroenterol Hepatol. 2003; 18: 386-392.
83. Schuppan D, Krebs A, Bauer M, Hahn EG. Hepatitis C and liver fibrosis. Cell Death Differ. 2003; 10:S59-S67.
84. Trakatelli C, Frydas S, Hatzistilianou M, Papadopoulos E, Simeonidou I, Founta A, Paludi D, Petrarca C, Castellani ML, Papaioannou N, Salini V, Conti P, Kempuraj D, Vecchiet J. Chemokines as markers for parasite-induced inflammation and tumors. Int J Biol Markers. 2005; 20:197-203.