Structural proteins of Hepatitis C virus induce interleukin 8 production and apoptosis in human endothelial cells

Journal of General Virology

Volumn 86, Issue 12, 2005, Pages 3291-3301

  Balasubramanian, Anuradha ^a   Munshi, Neru ^a   Koziel, Margaret J ^a   Hu, Zongyi ^b   Liang, T Jake ^b   Groopman, Jerome E ^a   Ganju, Ramesh K ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID DERIVATIVE; BETA GLUCURONIDASE; CASPASE 3; CASPASE 3 INHIBITOR; CHEMOKINE RECEPTOR; FAS ANTIGEN; FAS LIGAND; FLUORINE DERIVATIVE; GLUTAMIC ACID DERIVATIVE; I KAPPA B; INTERLEUKIN 8; KETONE; METHYL GROUP; NEUTRALIZING ANTIBODY; STRUCTURAL PROTEIN; VALINE; VIRUS PROTEIN;

APOPTOSIS; ARTICLE; BACULOVIRUS; BYSTANDER EFFECT; CELL ASSAY; CELL FUNCTION; CELL MIGRATION; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENDOTHELIUM CELL; ENZYME ACTIVATION; EXPOSURE; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR BLOCKING; SUPERNATANT; UMBILICAL VEIN; VIRUS PARTICLE;

ANTIGENS, CD95; APOPTOSIS; CASPASE 3; CASPASES; CELL MIGRATION INHIBITION; CELLS, CULTURED; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; FAS LIGAND PROTEIN; HEPACIVIRUS; HUMANS; INTERLEUKIN-8; MEMBRANE GLYCOPROTEINS; NF-KAPPA B; TUMOR NECROSIS FACTORS; VIRAL STRUCTURAL PROTEINS; VIROSOMES;

HEPATITIS C VIRUS;

EID: 28044453079     PISSN: 00221317     EISSN: None     Source Type: Journal    
DOI: 10.1099/vir.0.81056-0     Document Type: Article

References (65)

1. Adams, D. H. & Lloyd, A. R. (1997). Chemokines: leucocyte recruitment and activation cytokines. Lancet 349, 490-495.
2. Ameisen, J. C., Estaquier, J., Idziorek, T. & De Bels, F. (1995). Programmed cell death and AIDS pathogenesis: significance and potential mechanisms. Curr Top Microbiol Immunol 200, 195-211.
3. Baggiolini, M., Dewald, B. & Moser, B. (1994). Interleukin-8 and related chemotactic cytokines - CXC and CC chemokines. Adv Immunol 55, 97-179.
4. Balasubramanian, A., Ganju, R. K. & Groopman, J. E. (2003). Hepatitis C virus and HIV envelope proteins collaboratively mediate IL-8 secretion through activation of p38 MAP kinase and SHP2 in hepatocytes. J Biol Chem 278, 35755-35766.
5. Baltus, T., Weber, K. S., Johnson, Z., Proudfoot, A. E. & Weber, C. (2003). Oligomerization of RANTES is required for CCR1-mediated arrest but not CCR5-mediated transmigration of leukocytes on inflamed endothelium. Blood 102, 1985-1988.
6. Banda, N. K., Bernier, J., Kurahara, D. K., Kurrle, R., Haigwood, N., Sekaly, R. P. & Finkel, T. H. (1992). Crosslinking CD4 by human immunodeficiency virus gp120 primes T cells for activation-induced apoptosis. J Exp Med 176, 1099-1106.
7. Bashirova, A. A., Geijtenbeek, T. B., van Duijnhoven, G. C. & 10 other authors (2001). A dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin (DC-SIGN)-related protein is highly expressed on human liver sinusoidal endothelial cells and promotes HIV-1 infection. J Exp Med 193, 671-678.
8. Baumert, T. F., Ito, S., Wong, D. T. & Liang, T. J. (1998). Hepatitis C virus structural proteins assemble into virus-like particles in insect cells. J Virol 72, 3827-3836.
9. Baumert, T. F., Vergalla, J., Satoi, J., Thomson, M., Lechmann, M., Herion, D., Greenberg, H. B., Ito, S. & Liang, T. J. (1999). Hepatitis C virus-like particles synthesized in insect cells as a potential vaccine candidate. Gastroenterology 117, 1397-1407.
10. Boyum, A., Lovhaug, D., Tresland, L. & Nordlie, E. M. (1991). Separation of leukocytes: improved cell purity by fine adjustments of gradient medium density and osmolality. Scand J Immunol 34, 697-712.
11. Campbell, D. J., Kim, C. H. & Butcher, E. C. (2003). Chemokines in the systemic organization of immunity. Immunol Rev 195, 58-71.
12. Chinnaiyan, A. M., O'Rourke, K., Tewari, M. & Dixit, V. M. (1995). FADD, a novel death domain-containing protein, interacts with the death domain of Fas and initiates apoptosis. Cell 81, 505-512.
13. Choo, O. L., Kuo, G., Weiner, A. J., Overby, L. R., Bradley, D. W. & Houghton, M. (1989). Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science 244, 359-362.
14. Detmers, P. A., Powell, D. E., Walz, A., Clark-Lewis, I., Baggiolini, M. & Cohn, Z. A. (1991). Differential effects of neutrophil-activating peptide 1/IL-8 and its homologues on leukocyte adhesion and phagocytosis. J Immunol 147, 4211-4217.
15. Fukuda, R., Ishimura, N., Ishihara, S. & 11 other authors (1996). Intrahepatic expression of pro-inflammatory cytokine mRNAs and interferon efficacy in chronic hepatitis C. Liver 16, 390-399.
16. Gardner, J. P., Durso, R. J., Arrigale, R. R., Donovan, G. P., Maddon, P. J., Dragic, T. & Olson, W. C. (2003). L-SIGN (CD 209L) is a liver-specific capture receptor for hepatitis C virus. Proc Natl Acad Sci U S A 100, 4498-4503.
17. Grant, A. J., Goddard, S., Ahmed-Choudhury, J., Reynolds, G., Jackson, D. G., Briskin, M., Wu, L., Hubscher, S. G. & Adams, D. H. (2002). Hepatic expression of secondary lymphoid chemokine (CCL21) promotes the development of portal-associated lymphoid tissue in chronic inflammatory liver disease. Am J Pathol 160, 1445-1455.
18. + T cells from human immunodeficiency virus-infected asymptomatic individuals. J Exp Med 175, 331-340.
19. Heydtmann, M., Shields, P., McCaughan, G. & Adams, D. (2001). Cytokines and chemokines in the immune response to hepatitis C infection. Curr Opin Infect Dis 14, 279-287.
20. Hiramatsu, N., Hayashi, N., Katayama, K., Mochizuki, K., Kawanishi, Y., Kasahara, A., Fusamoto, H. & Kamada, T. (1994). Immunohistochemical detection of Fas antigen in liver tissue of patients with chronic hepatitis C. Hepatology 19, 1354-1359.
21. Hoofnagle, J. H. (1997). Hepatitis C: the clinical spectrum of disease. Hepatology 26, 15S-20S.
22. Huang, M. B., Hunter, M. & Bond, V. C. (1999). Effect of extracellular human immunodeficiency virus type 1 glycoprotein 120 on primary human vascular endothelial cell cultures. AIDS Res Hum Retroviruses 15, 1265-1277.
23. Johnston, B. & Butcher, E. C. (2002). Chemokines in rapid leukocyte adhesion triggering and migration. Semin Immunol 14, 83-92.
24. Jones, S. A., Dewald, B., Clark-Lewis, I. & Baggiolini, M. (1997). Chemokine antagonists that discriminate between interleukin-8 receptors. Selective blockers of CXCR2. J Biol Chem 272, 16166-16169.
25. Kaplanski, G., Farnarier, C., Payan, M. J., Bongrand, P. & Durand, J. M. (1997). 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 42, 2277-2284.
26. Kato, N., Hijikata, M., Ootsuyama, Y., Nakagawa, M., Ohkoshi, S., Sugimura, T. & Shimotohno, K. (1990). Molecular cloning of the human hepatitis C virus genome from Japanese patients with non-A, non-B hepatitis. Proc Natl Acad Sci U S A 87, 9524-9528.
27. Kim, D. W., Suzuki, R., Harada, T., Saito, I. & Miyamura, T. (1994). Trans-suppression of gene expression by hepatitis C viral core protein. Jpn J Med Sci Biol 47, 211-220.
28. Koziel, M. J., Dudley, D., Afdhal, N., Grakoui, A., Rice, C. M., Choo, Q. L., Houghton, M. & Walker, B. D. (1995). HLA class I-restricted cytotoxic T lymphocytes specific for hepatitis C virus. Identification of multiple epitopes and characterization of patterns of cytokine release. J Clin Invest 96, 2311-2321.
29. Lerat, H., Berby, F., Trabaud, M. A., Vidalin, O., Major, M., Trepo, C. & Inchauspe, G. (1996). Specific detection of hepatitis C virus minus strand RNA in hematopoietic cells. J Clin Invest 97, 845-851.
30. Loetscher, P., Seitz, M., Clark-Lewis, I., Baggiolini, M. & Moser, B. (1994). Both interleukin-8 receptors independently mediate chemotaxis. Jurkat cells transfected with IL-8R1 or IL-8R2 migrate in response to IL-8, GRO alpha and NAP-2. FEBS Lett 341, 187-192.
31. Lory, J. & Zimmermann, A. (1997). Endotheliitis-like changes in chronic hepatitis C. Histol Histopathol 12, 359-366.
32. Lozach, P. Y., Lortat-Jacob, H., de Lacroix de Lavalette, A. & 9 other authors (2003). DC-SIGN and L-SIGN are high affinity binding receptors for hepatitis C virus glycoprotein E2. J Biol Chem 278, 20358-20366.
33. Ludwig, I. S., Lekkerkerker, A. N., Depla, E., Bosman, F., Musters, R. J. P., Depraetere, S., van Kooyk, Y. & Geijtenbeek, T. B. H. (2004). Hepatitis C virus targets DC-SIGN and L-SIGN to escape lysosomal degradation. J Virol 78, 8322-8332.
34. Luster, A. D. (1998). Chemokines - chemotactic cytokines that mediate inflammation. N Engl J Med 338, 436-445.
35. Mackay, C. R. (1996). Chemokine receptors and T cell chemotaxis. J Exp Med 184, 799-802.
36. Mahmood, S., Sho, M., Yasuhara, Y. & 7 other authors (2002). Clinical significance of intrahepatic interleukin-8 in chronic hepatitis C patients. Hepatol Res 24, 413-419.
37. Masumoto, T., Ohkubo, K., Yamamoto, K., Ninomiya, T., Abe, M., Akbar, S. M., Michitaka, K., Horiike, N. & Onji, M. (1998). Serum IL-8 levels and localization of IL-8 in liver from patients with chronic viral hepatitis. Hepatogastroenterology 45, 1630-1634.
38. Meyaard, L., Otto, S. A., Jonker, R. R., Mijnster, M. J., Keet, R. P. & Miedema, F. (1992). Programmed death of T cells in HIV-I infection. Science 257, 217-219.
39. Miyamura, T. & Matsuura, Y. (1993). Structural proteins of hepatitis C virus. Trends Microbiol 1, 229-231.
40. Munshi, N., Balasubramanian, A., Koziel, M., Ganju, R. K. & Groopman, J. E. (2003). Hepatitis C and HIV envelope proteins cooperatively induce hepatocytic apoptosis via an innocent bystander mechanism. J Infect Dis 188, 1192-1204.
41. Murphy, P. M. (1997). Neutrophil receptors for interleukin-8 and related CXC chemokines. Semin Hematol 34, 311-318.
42. Muzio, M., Chinnaiyan, A. M., Kischkel, F. C. & 11 other authors (1996). FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex. Cell 85, 817-827.
43. Napoli, J., Bishop, G. A. & McCaughan, G. W. (1994). Increased intrahepatic messenger RNA expression of interleukins 2, 6, and 8 in human cirrhosis. Gastroenterology 107, 789-798.
44. + T cells and rapid elimination of effector cells by apoptosis. Eur J Immunol 28, 3448-3455.
45. Ohsawa, M., Shingu, N., Miwa, H., Yoshihara, H., Kubo, M., Tsukuma, H., Teshima, H., Hashimoto, M. & Aozasa, K. (1999). Risk of non-Hodgkin's lymphoma in patients with hepatitis C virus infection. Int J Cancer 80, 237-239.
46. Okuda, K. (1997). Hepatitis C and hepatocellular carcinoma. In Liver Cancer, pp. 38-50. Edited by K. Okuda & E. Tabor. London: Churchill Livingstone.
47. + T cells apoptosis: a possible mechanism of bystander cell death in HIV infection. J Immunol 158, 2456-2463.
48. Pohlmann, S., Soilleux, E. J., Baribaud, F., Leslie, G. J., Morris, L. S., Trowsdale, J., Lee, B., Coleman, N. & Doms, R. W. (2001). DC-SIGNR, a DC-SIGN homologue expressed in endothelial cells, binds to human and simian immunodeficiency viruses and activates infection in trans. Proc Natl Acad Sci U S A 98, 2670-2675.
49. Pohlmann, S., Zhang, J., Baribaud, F. & 7 other authors (2003). Hepatitis C virus glycoproteins interact with DC-SIGN and DC-SIGNR. J Virol 77, 4070-4080.
50. Poynard, T., Bedossa, P. & Opolon, P. (1997). Natural history of liver fibrosis progression in patients with chronic hepatitis C. The OBSVIRC, METAVIR, CLINIVIR, and DOSVIRC groups. Lancet 349, 825-832.
51. Rainger, G. E., Rowley, A. F. & Nash, G. B. (1998). Adhesion-dependent release of elastase from human neutrophils in a novel, flow-based model: specificity of different chemotactic agents. Blood 92, 4819-4827.
52. Ray, R. B., Lagging, L. M., Meyer, K., Steele, R. & Ray, R. (1995). Transcriptional regulation of cellular and viral promoters by the hepatitis C virus core protein. Virus Res 37, 209-220.
53. Ray, R. B., Steele, R., Meyer, K. & Ray, R. (1997). Transcriptional repression of p53 promoter by hepatitis C virus core protein. J Biol Chem 272, 10983-10986.
54. Roberts, J. M., Searle, J. W. & Cooksley, W. G. (1993). Histological patterns of prolonged hepatitis C infection. Gastroenterol Jpn 28, (Suppl. 5) 37-41.
55. Ruggieri, A., Harada, T., Matsuura, Y. & Miyamura, T. (1997). Sensitization to Fas-mediated apoptosis by hepatitis C virus core protein. Virology 229, 68-76.
56. Saito, I., Miyamura, T., Ohbayashi, A. & 8 other authors (1990). Hepatitis C virus infection is associated with the development of hepatocellular carcinoma. Proc Natl Acad Sci U S A 87, 6547-6549.
57. Shields, P. L., Morland, C. M., Salmon, M., Qin, S., Hubscher, S. G. & Adams, D. H. (1999). Chemokine and chemokine receptor interactions provide a mechanism for selective T cell recruitment to specific liver compartments within hepatitis C-infected liver. J Immunol 163, 6236-6243.
58. Shimoda, K., Begum, N. A., Shibuta, K., Mori, M., Bonkovsky, H. L., Banner, B. F. & Barnard, G. F. (1998). Interleukin-8 and hIRH (SDF1-α/PBSF) mRNA expression and histological activity index in patients with chronic hepatitis C. Hepatology 28, 108-115.
59. Smith, W. B., Gamble, J. R., Clark-Lewis, I. & Vadas, M. A. (1991). Interleukin-8 induces neutrophil transendothelial migration. Immunology 72, 65-72.
60. Tong, M. J., el-Farra, N. S., Reikes, A. R. & Co, R. L. (1995). Clinical outcomes after transfusion-associated hepatitis C. N Engl J Med 332, 1463-1466.
61. Trepo, C., Berthillon, P. & Vitvitski, L. (1998). HCV and lymphoproliferative diseases. Ann Oncol 9, 469-470.
62. Unutmaz, D., Pileri, P. & Abrignani, S. (1994). Antigen-independent activation of naive and memory resting T cells by a cytokine combination. J Exp Med 180, 1159-1164.
63. Volpes, R., Van den Oord, J. J. & Desmet, V. J. (1992). Vascular adhesion molecules in acute and chronic liver inflammation. Hepatology 15, 269-275.
64. Wolf, B. B. & Green, D. R. (1999). Suicidal tendencies: apoptotic cell death by caspase family proteinases. J Biol Chem 274, 20049-20052.
65. Zignego, A. L., Macchia, D., Monti, M. & 7 other authors (1992). Infection of peripheral mononuclear blood cells by hepatitis C virus. J Hepatol 15, 382-386.