Activation of hepatic stellate cells after phagocytosis of lymphocytes: A novel pathway of fibrogenesis

Hepatology

Volumn 48, Issue 3, 2008, Pages 963-977

  Muhanna, Nidal ^a   Doron, Sarit ^a   Wald, Ori ^a   Horani, Amjad ^a   Eid, Ahmed ^a   Pappo, Orit ^a   Friedman, Scott L ^b   Safadi, Rifaat ^a,c  

^a HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^b Division of Liver Diseases   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; INTEGRIN; INTERCELLULAR ADHESION MOLECULE 1; PROTEIN CDC42; RAC1 PROTEIN;

ADULT; ARTICLE; CD4 CD8 RATIO; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL IMMORTALIZATION; CELL INTERACTION; CLINICAL ARTICLE; COCULTURE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FEMALE; FIBRIN FORMATION; HEPATITIS B; HEPATITIS C; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL; LIVER CELL CULTURE; LIVER FIBROSIS; LYMPHOCYTE; LYMPHOCYTE SUBPOPULATION; LYMPHOCYTIC INFILTRATION; MALE; NATURAL KILLER CELL; PHAGOCYTOSIS; PRIORITY JOURNAL; REGULATORY MECHANISM; STELLATE CELL; TISSUE SECTION;

ADULT; BIOPSY; CASE-CONTROL STUDIES; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CDC42 GTP-BINDING PROTEIN; CELL COMMUNICATION; CELL LINE; CELLS, CULTURED; COCULTURE TECHNIQUES; FEMALE; HEPATITIS B, CHRONIC; HEPATITIS C, CHRONIC; HEPATOCYTES; HUMANS; KILLER CELLS, NATURAL; LIVER; LIVER CIRRHOSIS; MALE; MIDDLE AGED; PHAGOCYTOSIS; RAC1 GTP-BINDING PROTEIN;

EID: 51349102719     PISSN: 02709139     EISSN: None     Source Type: Journal    
DOI: 10.1002/hep.22413     Document Type: Article

References (70)

1. Wake K. Cell-cell organization and functions of 'sinusoids' in liver microcirculation system. J Electron Microsc (Tokyo) 1999;48:89-98.
2. Gressner A, Bachem M. Cellular sources of noncollagenous matrix proteins: Role of fatscoring cells in fibrogenesis. Semin Liver Dis 1990;10:30-46.
3. Pinzani M, Gesualdo L, Sabbah G, Abboud H. Effects of platelet-derived growth factor and other polypeptide mitogens on DNA synthesis and growth of cultured rat liver fatstoring cells. J Clin Invest 1989;84:1786-1793.
4. Matsuoka M, Tsukamoto H. Stimulation of hepatic lipocyte collagen production by Kupffer cell-derived transforming growth factor beta: implication for a pathogenetic role in alcoholic liver fibrogenesis. HEPATOLOGY 1990;11:599-605.
5. Reiter Z. Interferon: A major regulator of natural killer cell-mediated cytotoxicity. J Interferon Res 1993;13:247-257.
6. Cramp ME, Rossol S, Chokshi S, Carucci P, Williams R, Naoumov NV. Hepatitis C virus-specific T-cell reactivity during interferon and ribavirin treatment in chronic hepatitis C. Gastroenterology 2000;118:346-355.
7. Thimme R, Oldach D, Chang K, Steiger C, Ray SC, Chisati FV. Determinants of viral clearance and persistence during acute hepatitis C virus infection. J Exp Med 2001;194:1395-1406.
8. Grun̈er NH, Gerlach TJ, Jung M, Diepolder HM, Schirren CA, Schraut WW, et al. Association of hepatitis C virus-specific CD8+ T cells with viral clearance in acute hepatitis C. J Infect Dis 2000;181:1528-1536.
9. Koziel M. Cytokines in viral hepatitis. Semin Liver Dis 1999;19:157-169.
10. Brown PMJ, Neuman MG. Immunopathogenesis of hepatitis C viral infection: H1/TH2 responses and the role of cytokines. Clin Biochem 2001; 34:167-171.
11. Iredale JP. Hepatic stellate cell behavior during resolution of liver injury. Semin Liver Dis 2001;21:427-435.
12. Nelson DR, Marousis CG, Davis GL, Rice CM, Wong J, Houghton M, et al. The role of hepatitis C virus-specific cytotoxic T lymphocytes in chronic hepatitis C. J Immunol 1997;1;158:1473-1481.
13. Napoli J, Bishop G, McGuinness P, Painter D, McCaughan G. Progressive liver injury in chronic hepatitis C infection correlates with increased intrahepatic expression of Th1-associated cytokines. HEPATOLOGY 1996;24: 759-765.
14. Roger PM, Chaillou S, Breittmayer JP, Dahman M, St Paul MC, Chevallier P, et al. Intrahepatic CD4 T-cell apoptosis is related to METAVIR score in patients with chronic hepatitis C virus. Scand J Immunol 2005; 62:168-175.
15. Winau F, Hegasy G, Weiskirchen R, Weber S, Cassan C, Sieling PA, et al. Ito cells are liver-resident antigen-presenting cells for activating T cell responses. Immunity 2007;26:117-129.
16. Vinas O, Bataller R, Sancho-Bru P, Gines P, Berenguer C, Enrich C, et al. Human hepatic stellate cells show features of antigen-presenting cells and stimulate lymphocyte proliferation. HEPATOLOGY 2003;38:919-929.
17. Zhan SS, Jiang JX, Wu J, Halsted C, Friedman SL, Zern MA, et al. Phagocytosis of apoptotic bodies by hepatic stellate cells induces NADPH oxidase and is associated with liver fibrosis in vivo. HEPATOLOGY 2006;43: 435-443.
18. Safadi R, Ohta M, Alvarez CE, Fiel I, Barisal M, Mehal W, et al. Immune stimulation of hepatic fibrogenesis by CD8 lymphocytes and its attenuation by transgenic interleukin 10 from hepatocytes. Gastroenterology 2004;127:870-882.
19. Melhem A, Muhanna N, Bishara A, Alvarez CE, Ilan Y, Bishara T, et al. Anti-fibrotic activity of NK cells in experimental liver injury through killing of activated HSC. J Hepatol 2006;45:60-71.
20. Radaeva S, Sun R, Jaruga B, Nguyen VT, Tian Z, Gan B. Natural killer cells ameliorate liver fibrosis by killing activated stellate cells in NKG2D-dependent and tumor necrosis factor-related apoptosis-inducing ligand-dependent manners. Gastroenterology 2006;130:435-452.
21. Muhanna N, Horani A, Doron S, Safadi R. Lymphocyte-hepatic stellate cell proximity suggests a direct interaction. Clin Exp Immunol 2007;148: 338-347.
22. Bedossa P, Poynard T. An algorithm for the grading of activity in chronic hepatitis C: The METAVIR Cooperative Study Group. HEPATOLOGY 1996;24:289-293.
23. Boyum M. Isolation of mononuclear cells and granulocytes from human blood. Scand J Clin Lab Invest 1968;97:81-85.
24. Wald O, Pappo O, Safadi R, Dagan-Berger M, Beider K, Wald H, et al. Involvement of the CXCL12/CXCR4 pathway in the advanced liver disease that is associated with hepatitis C virus or hepatitis B virus. For J Immunol 2004;34:1164-1174.
25. Taimr P, Higuchi H, Kocova E, Rippe RA, Friedman S, Gores GJ. Activated human stellate cells express the TRAIL receptor-2/Death receptor-5 and undergo TRAIL-mediated apoptosis. HEPATOLOGY 2003;37:87-95.
26. Friedman SL, Rockey DC, McGuire RF, Maher JJ, Boyles JK, Yamasaki G. Isolated hepatic lipocytes and Kupffer cells from normal human liver: morphological and functional characteristics in primary culture. HEPATOLOGY 1992;15:234-243.
27. Hoppner M, Luhm J, Schlenke P, Koritke P, Frohn C. A flowcytometry based cytotoxicity assay using stained effector cells in combination with native target cells. J Immunol Methods 2002;15;267:157-163.
28. Qamar A, Sheikh SZ, Masud A, Jhandier MN, Inayat IB, Hakim W, et al. In vitro and in vivo protection of stellate cells from apoptosis by leptin. Dig Dis Sci 2006;51:1697-1705.
29. Forbes SJ, Russo FP, Rey V, Burra P, Rugge M, Wright NA, et al. A significant proportion of myofibroblasts are of bone marrow origin in human liver fibrosis. Gastroenterology 2004;126:955-963.
30. Sham RL, Packman CH, Abboud CN, Lichtman MA. Signal transduction and the regulation of actin conformation during myeloid maturation: Studies in HL60 cells. Blood 1991;77:363-370.
31. Brelje TC, Wessendorf MW, Sorenson RL. Multicolor laser scanning focal microscopy: Practical application and limitations. Methods Cell Biol 2002;70:165-244.
32. Tarshis M, Yavlovich A, Katzenell A, Ginsburg I, Rottem S. Intracellular location and survival of Mycoplasma penetrans within HeLa cells. Curr Microbiol 2004;49:136-140.
33. Inada S, Suzuki K, Kimura T, Hayashi A, Narita T, Yui R, et al. Concentric fibrosis and cellular infiltration around bile ducts induced by graft-versus-host reaction in mice: A role of CD8+ cells. Autoimmunity 1995;22:163-171.
34. Laso F, Iglesias-Osma C, Ciudad J, Lopez A, Pastor I, Orfao A. Chronic alcoholism is associated with an imbalanced production of Th-1/Th-2 cytokines by peripheral blood T cells. Alcohol Clin Exp Res 1999;23: 1306-1311.
35. Laso F, Iglesias-Osma C, Ciudad J, Lopez A, Pastor I, Torres E, et al. Alcoholic liver cirrhosis is associated with a decreased expression of the CD28 costimulatory molecule, a lower ability of T cells to bind exogenous IL-2, and increased soluble CD8 levels. Cycometry 2000;42:290-295.
36. Lombardo L, Capaldi A, Poccardi G, Vineis P. Peripheral blood CD3 and CD4 T-lymphocyte reduction correlates with severity of liver cirrhosis. Int J Clin Lab Res 1995;25:153-156.
37. Cougoule C, Wiedemann A, Lim J, Caron E. Phagocytosis, an alternative model system for the study of cell adhesion. Semin Cell Dev Biol 2004; 15:679-689.
38. Endo Y, Even-Ram S, Pankov R, Matsumoto K, Yamada KM. Inhibition of Rho GTPases by RNA Interference. Methods Enzymol 2006;406:345-361.
39. Valiante NM, D'Andrea A, Crotta S, Lechner F, Klenerman P, Nuti S, et al. Life, activation and death of intrahepatic lymphocytes in chronic hepatitis C. Immunol Rev 2000;174:77-89.
40. Mehal WZ, Azzaroli F, Crispe IN. Immunology of the healthy liver: Old questions and new insights. Gastroenterology 2001;120:250-260.
41. Lechner F, Wong DK, Dunbar PR, Chapman R, Chung RT, Dohrenwend P, et al. Analysis of successful immune responses in persons infected with hepatitis C virus. J Exp Med 2000;191:1499-1512.
42. Cooper S, Erickson AL, Adams EJ, Kansopon J, Weiner AJ, Chien DY, et al. Analysis of a successful immune response against hepatitis C virus. Immunity 1999;10:439-449.
43. Takaki A, Wiese M, Maertens G, Depla E, Seifert U, Liebetrau A, et al. Cellular immune responses persist and humoral responses decrease two decades after recovery from a single-source outbreak of hepatitis C. Nat Med 2000;6:578-582.
44. Gerlach JT, Diepolder HM, Jung MC, Gruener NH, Schraut WW, Zachoval R, et al. Recurrence of hepatitis C virus after loss of virus-specific CD4(+) T-cell response in acute hepatitis C. Gastroenterology 1999;117: 933-941.
45. Bertoletti A, D'Elios MM, Boni C, De Carli M, Zignego AL, Durazzo M, et al. Different cytokine profiles of intraphepatic T cells in chronic hepatitis B and hepatitis C virus infections. Gastroenterology 1997;112:193-199.
46. Ferrari C, Urbani S, Penna A, Cavalli A, Valli A, Lamonaca V, et al. Immunopathogenesis of hepatitis C virus infection. J Hepatol 1999; 31(Suppl 1):31-38.
47. Yao ZQ, Nguyen DT, Hiotellis AI, Hahn YS. Hepatitis C virus core protein inhibits human T lymphocyte responses by a complement-dependent regulatory pathway. J Immunol 2001;167:5264-5272.
48. Tran A, Yang G, Doglio A, Ticchioni M, Laffont C, Durant J, et al. Phenotyping of intrahepatic and peripheral blood lymphocytes in patients with chronic hepatitis C. Dig Dis Sci 1997;42:2495-2500.
49. Lanier LL. NK cell recognition. Ann Rev Immunol 2005;23:225-274.
50. Nattermann J, Feldmann G, Ahlenstiel G, Langhans B, Sauerbruch T, Spengler U. Surface expression and cytolytic function of NK cell receptors is altered in chronic hepatitis C. Gut 2006;55:869-877.
51. Morishima C, Paschal DM, Wang CC, Yoshihara CS, Wood BL, Yeo AE, et al. Decreased NK cell frequency in chronic hepatitis C does not affect ex vivo cytolytic killing. HEPATOLOGY 2006;43:573-580.
52. Lin AW, Gonzalez SA, Cunningham-Rundles S, Dorante G, Marshall S, Tignor A, et al. CD56(+dim) and CD56(+bright) cell activation and apoptosis in hepatitis C virus infection. Clin Exp Immunol 2004;137:408-416.
53. Meier UC, Owen RE, Taylor E, Worth A, Naoumov N, Willberg C, et al. Shared alterations in NK cell frequency, phenotype, and function in chronic human immunodeficiency virus and hepatitis C virus infections. J Virol 2005;79:12365-12374.
54. Par G, Rukavina D, Podack ER, Horanyi M, Szekeres-Bartho J, Hegedus G, et al. Decrease in CD3-negative-CD8dim(+) and Vdelta2/Vgamma9 TcR+ peripheral blood lymphocyte counts, low perforin expression and the impairment of natural killer cell activity is associated with chronic hepatitis C virus infection. J Hepatol 2002;37:514-522.
55. Deignan T, Curry MP, Doherty DG, Golden-Mason L, Volkov Y, Norris S, et al. Decrease in hepatic CD56(+) T cells and V alpha 24(+) natural killer T cells in chronic hepatitis C viral infection. J Hepatol 2002;37:101-108.
56. Kawarabayashi N, Seki S, Hatsuse K, Ohkawa T, Koike Y, Aihara T, et al. Decrease of CD56(+)T cells and natural killer cells in cirrhotic livers with hepatitis C may be involved in their susceptibility to hepatocellular carcinoma. HEPATOLOGY 2000;32:962-969.
57. Matheson DS, Green BJ, Minuk GY. Natural killer-cell activity and the response to interferons alpha, beta, and gamma in patients with primary biliary cirrhosis. J Allergy Clin Immunol 1989;84:214-218.
58. Corado J, Toro F, Rivera H, Bianco NE, Deibis L, De Sanctis JB. Impairment of natural killer (NK) cytotoxic activity in hepatitis C virus (HCV) infection. Clin Exp Immunol 1997;109:451-457.
59. Crotta S, Stilla A, Wack A, D'Andrea A, Nuti S, D'Oro U, et al. Inhibition of natural killer cells through engagement of CD81 by the major hepatitis C virus envelope protein. J Exp Med 2002;195:35-41.
60. 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.
61. Canbay A, Taimr P, Torok N, Higuchi H, Friedman S, Gores GJ. Apoptotic body engulfment by a human stellate cell line is profibrogenic. Lab Invest 2003;83:655-663.
62. Kosugi I, More H, Shirasawa H, Ito I. Endocytosis of soluble IgG immune complex and its transport to lysosomes in hepatic sinusoidal endothelial cells. J Hepatol 1992;16:106-114.
63. Hughes J, Liu Y, Van Damme J, Savill J. Human glomerular mesangial cell phagocytosis of apoptotic neutrophils. J Immunol 1997;158:4389-4397.
64. Savill J, Fadok V. Corpse clearance defines the meaning of cell death. Nature 2000;407:784-788.
65. Diamond MS, Garcia-Aguilar J, Bickford JK, Corbi AL, Springer TA. The I domain is a major recognition site on the leukocyte integrin Mac-1 (CD11b/CD18) for four distinct adhesion ligands. J Cell Biol 1993;120:1031-1043.
66. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998;19;392:245-252.
67. Etienne-Manneville S, Hall A. Rho GTPases in cell biology. Nature 2002; 420:629-635.
68. Fukata M, Kaibuchi K. Rho-family GTPases in cadherin-mediated cell-cell adhesion. Nat Rev Mol Cell Biol 2001;2:887-897.
69. Huynh ML, Fadok VA, Henson PM. Phosphatidylserine-dependent ingestion of apoptotic cells promotes TGF-beta1 secretion and the resolution of inflammation. J Clin Invest 2002;109:41-50.
70. Hoffmann PR, Kench JA, Vondracek A, Kruk E, Daleke DL, Jordan M, et al. Interaction between phosphatidylserine and the phosphatidylserine receptor inhibits immune responses in vivo. J Immunol 2005;174:1393-1404.