P-Selectin Suppresses Hepatic Inflammation and Fibrosis in Mice by Regulating Interferon γ and the IL-13 Decoy Receptor

Hepatology

Volumn 39, Issue 3, 2004, Pages 676-687

  Wynn, Thomas A ^a   Hesse, Matthias ^a,d   Sandler, Netanya G ^a   Kaviratne, Mallika ^a   Hoffmann, Karl F ^a,e   Chiaramonte, Monica G ^a,f   Reiman, Rachael ^a   Cheever, Allen W ^b   Sypek, Joseph P ^c   Mentink Kane, Margaret M ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b BIOMEDICAL RESEARCH INSTITUTE   (United States)

^c PFIZER INC   (United States)

^d Department of Obstetrics Gynecology   (United States)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^f Division of Immunobiology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; COLLAGEN; CYTOKINE; GAMMA INTERFERON; IMMUNOGLOBULIN FC FRAGMENT; INTERLEUKIN 13; INTERLEUKIN 13 ALPHA 2; INTERLEUKIN 13 RECEPTOR; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; PADGEM PROTEIN; RECEPTOR SUBTYPE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE COURSE; FEMALE; GENE DELETION; GRANULOMA; HEPATITIS; HISTOPATHOLOGY; INFLAMMATION; LEUKOCYTE MIGRATION; LIVER FIBROSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; RECEPTOR UPREGULATION; REGULATORY MECHANISM; SCHISTOSOMA MANSONI; TISSUE REPAIR; WILD TYPE;

ANIMALS; ANTIBODIES, MONOCLONAL; CHRONIC DISEASE; CYTOKINES; EOSINOPHILIA; FEMALE; GRANULOMA, RESPIRATORY TRACT; HEPATITIS; INTERFERON TYPE II; INTERLEUKIN-13 RECEPTOR ALPHA1 SUBUNIT; LIVER CIRRHOSIS; LUNG DISEASES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; P-SELECTIN; PROTEIN ISOFORMS; RECEPTORS, INTERLEUKIN; RECEPTORS, INTERLEUKIN-13; SCHISTOSOMIASIS;

EID: 12144290869     PISSN: 02709139     EISSN: None     Source Type: Journal    
DOI: 10.1002/hep.20102     Document Type: Article

References (50)

1. Wynn TA. IL-13 effector functions. Annu Rev Immunol 2003;21:425-456.
2. Hoffmann KF, Cheever AW, Wynn TA. 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.
3. Hoffmann KF, McCarty TC, Segal DH, Chiaramonte M, Hesse M, Davis EM, Cheever AW, et al. Disease fingerprinting with cDNA microarrays reveals distinct gene expression profiles in lethal type 1 and type 2 cytokine-mediated inflammatory reactions. FASEB J 2001;15:2545-2547.
4. Chiaramonte MG, Donaldson DD, Cheever AW, Wynn TA. An IL-13 inhibitor blocks the development of hepatic fibrosis during a T-helper type 2-dominated inflammatory response. J Clin Invest 1999;104:777-785.
5. Chiaramonte MG, Cheever AW, Malley JD, Donaldson DD, Wynn TA. Studies of murine schistosomiasis reveal interleukin-13 blockade as a treatment for established and progressive liver fibrosis. HEPATOLOGY 2001;34:273-282.
6. Fallon PG, Richardson EJ, McKenzie GJ, McKenzie AN. Schistosome infection of transgenic mice defines distinct and contrasting pathogenic roles for IL-4 and IL-13: IL-13 is a profibrotic agent. J Immunol 2000;164:2585-2591.
7. Wynn TA, Cheever AW, Jankovic D, Poindexter RW, Caspar P, Lewis FA, Sher A. An IL-12-based vaccination method for preventing fibrosis induced by schistosome infection. Nature 1995;376:594-596.
8. Kaplan MH, Whitfield JR, Boros DL, Grusby MJ. Th2 cells are required for the Schistosoma mansoni egg-induced granulomatous response. J Immunol 1998;160:1850-1856.
9. Pearce EJ, Cheever A, Leonard S, Covalesky M, Fernandez-Botran R, Kohler G, Kopf M. Schistosoma mansoni in IL-4-deficient mice. Int Immunol 1996;8:435-444.
10. Jankovic D, Kullberg MC, Noben-Trauth N, Caspar P, Ward JM, Cheever AW, Paul WE, et al. Schistosome-infected IL-4 receptor knock-out (KO) mice, in contrast to IL-4 KO mice, fail to develop granulomatous pathology while maintaining the same lymphokine expression profile. J Immunol 1999;163:337-342.
11. Kansas GS. Selectins and their ligands: current concepts and controversies. Blood 1996;88:3259-3287.
12. Wardlaw AJ. Eosinophil trafficking in asthma. Clin Med 2001;1:214-218.
13. Pober JS, Kluger MS, Schechner JS. Human endothelial cell presentation of antigen and the homing of memory/effector T cells to skin. Ann N Y Acad Sci 2001;941:12-25.
14. Steeber DA, Tedder TF. Adhesion molecule cascades direct lymphocyte recirculation and leukocyte migration during inflammation. Immunol Res 2000;22:299-317.
15. Austrup F, Vestweber D, Borges E, Lohning M, Brauer R, Herz U, Renz H, et al. P- and E-selectin mediate recruitment of T-helper-1 but not T-helper-2 cells into inflammed [sic] tissues. Nature 1997;385:81-83.
16. Borges E, Tietz W, Steegmaier M, Moll T, Hallmann R, Hamann A, Vestweber D. P-selectin glycoprotein ligand-1 (PSGL-1) on T helper 1 but not on T helper 2 cells binds to P-selectin and supports migration into inflamed skin. J Exp Med 1997;185:573-578.
17. Cheever AW, Williams ME, Wynn TA, Finkelman FD, Seder RA, Cox TM, Hieny S, et al. Anti-IL-4 treatment of Schistosoma mansoni-infected mice inhibits development of T cells and non-B, non-T cells expressing Th2 cytokines while decreasing egg-induced hepatic fibrosis. J Immunol 1994;153:753-759.
18. Donaldson DD, Whitters MJ, Fitz LJ, Neben TY, Finnerty H, Henderson SL, O'Hara RM Jr, et al. The murine IL-13 receptor alpha 2: molecular cloning, characterization, and comparison with murine IL-13 receptor alpha 1. J Immunol 1998;161:2317-2324.
19. Hesse M, Modolell M, La Flamme AC, Schito M, Fuentes JM, Cheever AW, Pearce EJ, 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.
20. Wynn TA, Eltoum I, Oswald IP, Cheever AW, Sher A. Endogenous interleukin 12 (IL-12) regulates granuloma formation induced by eggs of Schistosoma mansoni and exogenous IL-12 both inhibits and prophylactically immunizes against egg pathology. J Exp Med 1994;179:1551-1561.
21. Arbones ML, Ord DC, Ley K, Ratech H, Maynard-Curry C, Otten G, Capon DJ, et al. Lymphocyte homing and leukocyte rolling and migration are impaired in L-selectin-deficient mice. Immunity 1994;1:247-260.
22. Kawakami K, Taguchi J, Murata T, Puri RK. The interleukin-13 receptor alpha2 chain: an essential component for binding and internalization but not for interleukin-13-induced signal transduction through the STAT6 pathway. Blood 2001;97:2673-2679.
23. Wood N, Whitters MJ, Jacobson BA, Witek J, Sypek JP, Kasaian M, Eppihimer MJ, et al. Enhanced interleukin (IL)-13 responses in mice lacking IL-13 receptor alpha 2. J Exp Med 2003;197:703-709.
24. Chiaramonte MG, Mentink-Kane M, Jacobson BA, Cheever AW, Whitters MJ, Goad ME, Wong A, et al. Regulation and function of the interleukin 13 receptor alpha 2 during a T helper cell type 2-dominant immune response. J Exp Med 2003;197:687-701.
25. Symon FA, Walsh GM, Watson SR, Wardlaw AJ. Eosinophil adhesion to nasal polyp endothelium is P-selectin-dependent. J Exp Med 1994;180:371-376.
26. Kitayama J, Fuhlbrigge RC, Puri KD, Springer TA. P-selectin, L-selectin, and alpha 4 integrin have distinct roles in eosinophil tethering and arrest on vascular endothelial cells under physiological flow conditions. J Immunol 1997;159:3929-3939.
27. Broide DH, Humber D, Sullivan S, Sriramarao P. Inhibition of eosinophil rolling and recruitment in P-selectin- and intracellular adhesion molecule-1-deficient mice. Blood 1998;91:2847-2856.
28. Robinson SD, Frenette PS, Rayburn H, Cummiskey M, Ullman-Cullere M, Wagner DD, Hynes RO. Multiple, targeted deficiencies in selectins reveal a predominant role for P-selectin in leukocyte recruitment. Proc Natl Acad Sci U S A 1999;96:11452-11457.
29. Woltmann G, McNulty CA, Dewson G, Symon FA, Wardlaw AJ. Interleukin-13 induces PSGL-1/P-selectin-dependent adhesion of eosinophils, but not neutrophils, to human umbilical vein endothelial cells under flow. Blood 2000;95:3146-3152.
30. Henriques GM, Miotla JM, Cordeiro SB, Wolitzky BA, Woolley ST, Hellewell PG. Selectins mediate eosinophil recruitment in vivo: a comparison with their role in neutrophil influx. Blood 1996;87:5297-5304.
31. Strauss EC, Larson KA, Brenneise I, Foster CS, Larsen GR, Lee NA, Lee JJ. Soluble P-selectin glycoprotein ligand 1 inhibits ocular inflammation in a murine model of allergy. Invest Ophthalmol Vis Sci 1999;40:1336-1342.
32. Wardlaw AJ. Molecular basis for selective eosinophil trafficking in asthma: a multistep paradigm. J Allergy Clin Immunol 1999;104:917-926.
33. Kaifi JT, Hall LR, Diaz C, Sypek J, Diaconu E, Lass JH, Pearlman E. Impaired eosinophil recruitment to the cornea in P-selectin-deficient mice in Onchocerca volvulus keratitis (River blindness). Invest Ophthalmol Vis Sci 2000;41:3856-3861.
34. Broide DH, Sullivan S, Gifford T, Sriramarao P. Inhibition of pulmonary eosinophilia in P-selectin- and ICAM-1-deficient mice. Am J Respir Cell Mol Biol 1998;18:218-225.
35. Steegmaier M, Blanks JE, Borges E, Vestweber D. P-selectin glycoprotein ligand-1 mediates rolling of mouse bone marrow-derived mast cells on P-selectin but not efficiently on E-selectin. Eur J Immunol 1997;27:1339-1345.
36. Sabin EA, Kopf MA, Pearce EJ. Schistosoma mansoni egg-induced early IL-4 production is dependent upon IL-5 and eosinophils. J Exp Med 1996;184:1871-1878.
37. Owhashi M, Horii Y, Ikeda T, Maruyama H, Abe T, Nawa Y. Importance of mast-cell derived eosinophil chemotactic factor A on granuloma formation in murine Schistosomiasis japonica: evaluation using mast-cell-deficient W/WV mice. Int Arch Allergy Appl Immunol 1990;92:64-68.
38. Cheever AW, Andrade ZA. Pathological lesions associated with Schistosoma mansoni infection in man. Trans R Soc Trop Med Hyg 1967;61:626-639.
39. Chiaramonte MG, Schopf LR, Neben TY, Cheever AW, Donaldson DD, Wynn TA. IL-13 is a key regulatory cytokine for Th2 cell-mediated pulmonary granuloma formation and IgE responses induced by Schistosoma mansoni eggs. J Immunol 1999;162:920-930.
40. Ruth JH, Warmington KS, Shang X, Lincoln P, Evanoff H, Kunkel SL, Chensue SW. Interleukin 4 and 13 participation in mycobacterial (type-1) and schistosomal (type-2) antigen-elicited pulmonary granuloma formation: multiparameter analysis of cellular recruitment, chemokine expression and cytokine networks. Cytokine 2000;12:432-444.
41. Kapp U, Yeh WC, Patterson B, Elia AJ, Kagi D, Ho A, Hessel A, et al. Interleukin 13 is secreted by and stimulates the growth of Hodgkin and Reed-Sternberg cells. J Exp Med 1999;189:1939-1946.
42. Wills-Karp M, Luyimbazi J, Xu X, Schofield B, Neben TY, Karp CL, Donaldson DD. Interleukin-13: central mediator of allergic asthma [see comments]. Science 1998;282:2258-2261.
43. Grunig G, Warnock M, Wakil AE, Venkayya R, Brombacher F, Rennick DM, Sheppard D, et al. Requirement for IL-13 independently of IL-4 in experimental asthma. Science 1998;232:2261-2263.
44. Hansen G, Berry G, DeKruyff RH, Umetsu DT. Allergen-specific Th1 cells fail to counterbalance Th2 cell-induced airway hyperreactivity but cause severe airway inflammation. J Clin Invest 1999;103:175-183.
45. Randolph DA, Stephens R, Carruthers CJ, Chaplin DD. Cooperation between Th1 and Th2 cells in a murine model of eosinophilic airway inflammation. J Clin Invest 1999;104:1021-1029.
46. Ford JG, Rennick D, Donaldson DD, Venkayya R, McArthur C, Hansell E, Kurup VP, et al. IL-13 and IFN-gamma: interactions in lung inflammation. J Immunol 2001;167:1769-1777.
47. Castro M, Chaplin DD, Walter MJ, Holtzman MJ. Could asthma be worsened by stimulating the T-helper type 1 immune response? Am J Respir Cell Mol Biol 2000;22:143-146.
48. Czaja MJ, Weiner FR, Takahashi S, Giambrone MA, van der Meide PH, Schellekens H, Biempica L, et al. Gamma-interferon treatment inhibits collagen deposition in murine schistosomiasis. Hepatology 1993;10:795-800.
49. Rosenkranz AR, Mendrick DL, Cotran RS, Mayadas TN. P-selectin deficiency exacerbates experimental glomerulonephritis: a protective role for endothelial P-selectin in inflammation. J Clin Invest 1999;103:649-659.
50. Bullard DC, Mobley JM, Justen JM, Sly LM, Chosay JG, Dunn CJ, Lindsey JR, et al. Acceleration and increased severity of collagen-induced arthritis in P-selectin mutant mice. J Immunol 1999;163:2844-2849.