Role of resident liver cells in the pathogenesis of schistosomiasis

Trends in Parasitology

Volumn 28, Issue 12, 2012, Pages 572-579

  Anthony, Barrie J ^a   Ramm, Grant A ^a,b   McManus, Donald P ^a  

^a ROYAL BRISBANE AND WOMEN'S HOSPITAL   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Hepatic stellate cells; Kupffer cells; Liver; Liver sinusoidal endothelial cells; Macrophages; Schistosoma japonicum; Schistosoma mansoni; Schistosomiasis

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN; CONNECTIVE TISSUE GROWTH FACTOR; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 4 RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA AGONIST; PRAZIQUANTEL; ROSIGLITAZONE; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1; VASCULOTROPIN;

ANGIOGENESIS; ANTIINFLAMMATORY ACTIVITY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELL PROLIFERATION; CELL TRANSDIFFERENTIATION; CHRONIC LIVER DISEASE; CYTOKINE PRODUCTION; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; FIBROBLAST; FIBROGENESIS; HEPATITIS; HUMAN; IMMUNOPATHOLOGY; INFLAMMATORY INFILTRATE; KUPFFER CELL; LIVER CELL; LIVER FIBROSIS; LIVER GRANULOMA; LIVER PROTECTION; LIVER SINUSOID; LIVER SINUSOIDAL ENDOTHELIAL CELL; MACROPHAGE ACTIVATION; MYOFIBROBLAST; NONHUMAN; PARASITE VIRULENCE; PATHOGENESIS; PHAGOCYTOSIS; PORTAL HYPERTENSION; RESIDENT LIVER CELL; RETICULOENDOTHELIAL SYSTEM; REVIEW; SCHISTOSOMA; SCHISTOSOMA JAPONICUM; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS; STELLATE CELL; TH1 CELL; TH2 CELL;

ENDOTHELIAL CELLS; HEPATIC STELLATE CELLS; HEPATOCYTES; HUMANS; KUPFFER CELLS; LIVER; LIVER DISEASES; SCHISTOSOMIASIS;

SCHISTOSOMA; SCHISTOSOMA JAPONICUM; SCHISTOSOMA MANSONI;

EID: 84869201986     PISSN: 14714922     EISSN: 14715007     Source Type: Journal    
DOI: 10.1016/j.pt.2012.09.005     Document Type: Review

References (86)

1. Crompton D.W. How much human helminthiasis is there in the world?. J. Parasitol. 1999, 85:397-403.
2. Chitsulo L., et al. The global status of schistosomiasis and its control. Acta Trop. 2000, 77:41-51.
3. King C.H., Dangerfield-Cha M. The unacknowledged impact of chronic schistosomiasis. Chronic Illn. 2008, 4:65-79.
4. King C.H., et al. Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet 2005, 365:1561-1569.
5. McManus D.P., et al. Schistosomiasis in the People's Republic of China: the era of the Three Gorges Dam. Clin. Microbiol. Rev. 2010, 23:442-466.
6. Wynn T.A., et al. Immunopathogenesis of schistosomiasis. Immunol. Rev. 2004, 201:156-167.
7. Gryseels B. Schistosomiasis. Infect. Dis. Clin. North Am. 2012, 26:383-397.
8. Burke M.L., et al. Immunopathogenesis of human schistosomiasis. Parasite Immunol. 2009, 31:163-176.
9. Liu T., et al. FIZZ1 stimulation of myofibroblast differentiation. Am. J. Pathol. 2004, 164:1315-1326.
10. Hesse M., et al. Differential regulation of nitric oxide synthase-2 and arginase-1 by type 1/type 2 cytokines in vivo: granulomatous pathology is shaped by the pattern of L-arginine metabolism. J. Immunol. 2001, 167:6533-6544.
11. H2 paradigm. Nat. Rev. Immunol. 2004, 4:583-594.
12. Booth M., et al. Periportal fibrosis in human Schistosoma mansoni infection is associated with low IL-10, low IFN-gamma, high TNF-alpha, or low RANTES, depending on age and gender. J. Immunol. 2004, 172:1295-1303.
13. de Jesus A.R., et al. Association of type 2 cytokines with hepatic fibrosis in human Schistosoma mansoni infection. Infect. Immun. 2004, 72:3391-3397.
14. Friedman S.L. Liver fibrosis - from bench to bedside. J. Hepatol. 2003, 38(Suppl. 1):S38-S53.
15. Bartley P.B., et al. A contributory role for activated hepatic stellate cells in the dynamics of Schistosoma japonicum egg-induced fibrosis. Int. J. Parasitol. 2006, 36:993-1001.
16. Chang D., et al. Hepatic stellate cells in human schistosomiasis mansoni: a comparative immunohistochemical study with liver cirrhosis. Acta Trop. 2006, 97:318-323.
17. Wallace K., et al. Liver fibrosis. Biochem. J. 2008, 411:1-18.
18. Smith P., et al. Schistosoma mansoni worms induce anergy of T cells via selective up-regulation of programmed death ligand 1 on macrophages. J. Immunol. 2004, 173:1240-1248.
19. Herbert D.R., et al. Alternative macrophage activation is essential for survival during schistosomiasis and downmodulates T helper 1 responses and immunopathology. Immunity 2004, 20:623-635.
20. Andrade Z.A., Santana T.S. Angiogenesis and schistosomiasis. Mem. Inst. Oswaldo Cruz 2010, 105:436-439.
21. Smedsrod B. Clearance function of scavenger endothelial cells. Comp. Hepatol. 2004, 3(Suppl. 1):S22.
22. Friedman S.L. Hepatic fibrosis - overview. Toxicology 2008, 254:120-129.
23. Ramm G.A. Chemokine (C-C motif) receptors in fibrogenesis and hepatic regeneration following acute and chronic liver disease. Hepatology 2009, 50:1664-1668.
24. Ramm G.A. Anti-chemokine therapy for the treatment of hepatic fibrosis: an attractive approach. Hepatology 2011, 54:354-358.
25. Ramm G.A., et al. Morphology of liver repair following cholestatic liver injury: resolution of ductal hyperplasia, matrix deposition and regression of myofibroblasts. Liver 2000, 20:387-396.
26. Issa R., et al. Apoptosis of hepatic stellate cells: involvement in resolution of biliary fibrosis and regulation by soluble growth factors. Gut 2001, 48:548-557.
27. Anthony B., et al. Hepatic stellate cells and parasite-induced liver fibrosis. Parasit Vectors 2010, 3:60.
28. Zou W.L., et al. Inhibitory effects of prostaglandin E1 on activation of hepatic stellate cells in rabbits with schistosomiasis. Hepatobiliary Pancreat. Dis. Int. 2007, 6:176-181.
29. Chatterjee S., et al. Circulating levels of the neuropeptide hormone somatostatin may determine hepatic fibrosis in Schistosoma mansoni infections. Acta Trop. 2004, 90:191-203.
30. Chatterjee S., et al. Does the neuropeptide somatostatin have therapeutic potential against schistosomiasis?. Trends Parasitol. 2002, 18:295-298.
31. Reynaert H., et al. Somatostatin suppresses endothelin-1-induced rat hepatic stellate cell contraction via somatostatin receptor subtype 1. Gastroenterology 2001, 121:915-930.
32. Potter J.J., et al. Influence of leptin in the development of hepatic fibrosis produced in mice by Schistosoma mansoni infection and by chronic carbon tetrachloride administration. J. Hepatol. 2003, 38:281-288.
33. Tang M., et al. Leptin enhances the effect of transforming growth factor beta in increasing type I collagen formation. Biochem. Biophys. Res. Commun. 2002, 297:906-911.
34. Lenzi H.L., et al. Four whole-istic aspects of schistosome granuloma biology: fractal arrangement, internal regulation, autopoietic component and closure. Mem. Inst. Oswaldo Cruz 2006, 101(Suppl. 1):219-231.
35. Tong Q.X., et al. Study on the effect of heluoshugan capsule on liver fibrosis induced by Schistosoma japonicum infection in mice. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 2006, 24:129-132. (in Chinese).
36. Chu D., et al. Paeoniflorin inhibits TGF-beta1-mediated collagen production by Schistosoma japonicum soluble egg antigen in vitro. Parasitology 2007, 134:1611-1621.
37. Fairfax K.C., et al. IL-10R blockade during chronic schistosomiasis mansoni results in the loss of B cells from the liver and the development of severe pulmonary disease. PLoS Pathog. 2012, 8:e1002490.
38. Wynn T.A. IL-13 effector functions. Annu. Rev. Immunol. 2003, 21:425-456.
39. Liu Y., et al. IL-13 induces connective tissue growth factor in rat hepatic stellate cells via TGF-beta-independent Smad signaling. J. Immunol. 2011, 187:2814-2823.
40. Sugimoto R., et al. Effect of IL-4 and IL-13 on collagen production in cultured LI90 human hepatic stellate cells. Liver Int. 2005, 25:420-428.
41. Liu Y., et al. IL-13 signaling in liver fibrogenesis. Front Immunol. 2012, 3:116.
42. Anthony B., et al. Schistosoma mansoni: egg-induced downregulation of hepatic stellate cell activation and fibrogenesis. Exp. Parasitol. 2010, 124:409-420.
43. Chen H., et al. Rosiglitazone prevents murine hepatic fibrosis induced by Schistosoma japonicum. World J. Gastroenterol. 2008, 14:2905-2911.
44. Anthony B.J., et al. A role for peroxisome proliferator-activated receptors in the immunopathology of schistosomiasis?. PPAR Res. 2012, 2012:128068.
45. Chan M.M., et al. Peroxisome proliferator-activated receptor (PPAR): balance for survival in parasitic infections. J. Biomed. Biotechnol. 2010, 2010:828951.
46. Bomble M., et al. Analysis of antigen-presenting functionality of cultured rat hepatic stellate cells and transdifferentiated myofibroblasts. Biochem. Biophys. Res. Commun. 2010, 396:342-347.
47. Vinas O., et al. Human hepatic stellate cells show features of antigen-presenting cells and stimulate lymphocyte proliferation. Hepatology 2003, 38:919-929.
48. Shen H., et al. Expression of Fc fragment receptors of immunoglobulin G (Fc gammaRs) in rat hepatic stellate cells. Dig. Dis. Sci. 2005, 50:181-187.
49. Forbes S.J., Parola M. Liver fibrogenic cells. Best Pract. Res. Clin. Gastroenterol. 2011, 25:207-217.
50. Guyot C., et al. Hepatic fibrosis and cirrhosis: the (myo)fibroblastic cell subpopulations involved. Int. J. Biochem. Cell Biol. 2006, 38:135-151.
51. Dranoff J.A., Wells R.G. Portal fibroblasts: underappreciated mediators of biliary fibrosis. Hepatology 2010, 51:1438-1444.
52. Adams D.H., et al. Mechanisms of immune-mediated liver injury. Toxicol. Sci. 2010, 115:307-321.
53. Mandal P., et al. Molecular mechanism for adiponectin-dependent M2 macrophage polarization: link between the metabolic and innate immune activity of full-length adiponectin. J. Biol. Chem. 2011, 286:13460-13469.
54. Odegaard J.I., et al. Alternative M2 activation of Kupffer cells by PPARdelta ameliorates obesity-induced insulin resistance. Cell Metab. 2008, 7:496-507.
55. Jenkins S.J., et al. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science 2011, 332:1284-1288.
56. Reyes J.L., Terrazas L.I. The divergent roles of alternatively activated macrophages in helminthic infections. Parasite Immunol. 2007, 29:609-619.
57. Cassetta L., et al. Macrophage polarization in health and disease. ScientificWorldJournal 2011, 11:2391-2402.
58. Loke P., et al. Alternatively activated macrophages induced by nematode infection inhibit proliferation via cell-to-cell contact. Eur. J. Immunol. 2000, 30:2669-2678.
59. Terrazas L.I., et al. Role of the programmed Death-1 pathway in the suppressive activity of alternatively activated macrophages in experimental cysticercosis. Int. J. Parasitol. 2005, 35:1349-1358.
60. Mejri N., Gottstein B. Intraperitoneal Echinococcus multilocularis infection in C57BL/6 mice affects CD40 and B7 costimulator expression on peritoneal macrophages and impairs peritoneal T cell activation. Parasite Immunol. 2006, 28:373-385.
61. Hoffmann K.F., et al. IL-10 and the dangers of immune polarization: excessive type 1 and type 2 cytokine responses induce distinct forms of lethal immunopathology in murine schistosomiasis. J. Immunol. 2000, 164:6406-6416.
62. Dewals B.G., et al. IL-4Ralpha-independent expression of mannose receptor and Ym1 by macrophages depends on their IL-10 responsiveness. PLoS Negl. Trop. Dis. 2010, 4:e689.
63. Flores Villanueva P.O., et al. Macrophages from schistosomal egg granulomas induce unresponsiveness in specific cloned Th-1 lymphocytes in vitro and down-regulate schistosomal granulomatous disease in vivo. J. Immunol. 1994, 152:1847-1855.
64. Bronte V., et al. L-arginine metabolism in myeloid cells controls T-lymphocyte functions. Trends Immunol. 2003, 24:302-306.
65. Connolly M.K., et al. In hepatic fibrosis, liver sinusoidal endothelial cells acquire enhanced immunogenicity. J. Immunol. 2010, 185:2200-2208.
66. Knolle P.A., Limmer A. Control of immune responses by scavenger liver endothelial cells. Swiss Med. Wkly. 2003, 133:501-506.
67. Warren A., et al. T lymphocytes interact with hepatocytes through fenestrations in murine liver sinusoidal endothelial cells. Hepatology 2006, 44:1182-1190.
68. Shariati F., et al. Evaluation of the role of angiogenic factors in the pathogenesis of schistosomiasis. Exp. Parasitol. 2011, 128:44-49.
69. Abdel Fattah N.S., Ahmed N.S. Evidence of intra-hepatic vascular proliferation remodeling early after cure in experimental schistosomiasis mansoni: an immunohistochemical descriptive study. Exp. Parasitol. 2012, 130:58-62.
70. Thabut D., Shah V. Intrahepatic angiogenesis and sinusoidal remodeling in chronic liver disease: new targets for the treatment of portal hypertension?. J. Hepatol. 2010, 53:976-980.
71. Fernandez M., et al. Angiogenesis in liver disease. J. Hepatol. 2009, 50:604-620.
72. Assy N., et al. Effect of vascular endothelial growth factor on hepatic regenerative activity following partial hepatectomy in rats. J. Hepatol. 1999, 30:911-915.
73. Taniguchi E., et al. Expression and role of vascular endothelial growth factor in liver regeneration after partial hepatectomy in rats. J. Histochem. Cytochem. 2001, 49:121-130.
74. Redaelli C.A., et al. Effect of vascular endothelial growth factor on functional recovery after hepatectomy in lean and obese mice. J. Hepatol. 2004, 40:305-312.
75. Loeffler D.A., et al. Soluble egg antigens from Schistosoma mansoni induce angiogenesis-related processes by up-regulating vascular endothelial growth factor in human endothelial cells. J. Infect. Dis. 2002, 185:1650-1656.
76. Tawfeek G.M., et al. Immunological indicators of morbidity in human schistosomiasis mansoni: role of vascular endothelial growth factor and anti-soluble egg antigen IgG4 in disease progression. J. Egypt Soc. Parasitol. 2003, 33:597-614.
77. Baptista A.P., Andrade Z.A. Angiogenesis and schistosomal granuloma formation. Mem. Inst. Oswaldo Cruz. 2005, 100:183-185.
78. Bamboat Z.M., et al. Human liver dendritic cells promote T cell hyporesponsiveness. J. Immunol. 2009, 182:1901-1911.
79. Everts B., et al. Omega-1, a glycoprotein secreted by Schistosoma mansoni eggs, drives Th2 responses. J. Exp. Med. 2009, 206:1673-1680.
80. Kane C.M., et al. Helminth antigens modulate TLR-initiated dendritic cell activation. J. Immunol. 2004, 173:7454-7461.
81. Perona-Wright G., et al. Dendritic cell activation and function in response to Schistosoma mansoni. Int. J. Parasitol. 2006, 36:711-721.
82. MacDonald A.S., et al. Cutting edge: Th2 response induction by dendritic cells: a role for CD40. J. Immunol. 2002, 168:537-540.
83. van Liempt E., et al. Schistosoma mansoni soluble egg antigens are internalized by human dendritic cells through multiple C-type lectins and suppress TLR-induced dendritic cell activation. Mol. Immunol. 2007, 44:2605-2615.
84. Burke M.L., et al. Temporal expression of chemokines dictates the hepatic inflammatory infiltrate in a murine model of schistosomiasis. PLoS Negl. Trop. Dis. 2010, 4:e598.
85. Cheng Y.L., et al. The effects of T cell deficiency on the development of worms and granuloma formation in mice infected with Schistosoma japonicum. Parasitol. Res. 2008, 102:1129-1134.
86. Mentink-Kane M.M., et al. IL-13 receptor alpha 2 down-modulates granulomatous inflammation and prolongs host survival in schistosomiasis. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:586-590.