Loss of discoidin domain receptor 2 promotes hepatic fibrosis after chronic carbon tetrachloride through altered paracrine interactions between hepatic stellate cells and liver-associated macrophages

American Journal of Pathology

Volumn 179, Issue 6, 2011, Pages 2894-2904

  Olaso, Elvira ^a,b   Arteta, Beatriz ^a   Benedicto, Aitor ^a   Crende, Olatz ^a   Friedman, Scott L ^b  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CARBON TETRACHLORIDE; COLLAGEN; COLLAGEN TYPE 1; COLLAGENASE 3; DESMIN; DISCOIDIN DOMAIN RECEPTOR 2; GELATINASE A; GELATINASE B; INTERLEUKIN 10; INTERLEUKIN 6; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; OSTEOPONTIN; RECEPTOR PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CELL MIGRATION; CELL PROLIFERATION; CHEMOTAXIS; CONTROLLED STUDY; CYTOKINE RELEASE; EXTRACELLULAR MATRIX; FIBROGENESIS; GENE EXPRESSION REGULATION; IN VITRO STUDY; INTRACELLULAR SIGNALING; LIVER FIBROSIS; LIVER INJURY; MACROPHAGE; MALE; MOUSE; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; STELLATE CELL;

ACUTE LUNG INJURY; ANIMALS; CARBON TETRACHLORIDE; CELL COMMUNICATION; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; COLLAGEN TYPE I; COLLAGENASES; GELATINASES; HEPATIC STELLATE CELLS; LIVER CIRRHOSIS; MACROPHAGES; MALE; MICE; MICE, KNOCKOUT; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, MITOGEN; SIGNAL TRANSDUCTION;

EID: 81255124245     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.09.002     Document Type: Article

References (38)

1. S.L. Friedman Liver fibrosisfrom bench to bedside J Hepatol 38 2003 S38 S53
2. R. Bataller, and D.A. Brenner Liver fibrosis J Clin Invest 115 2005 209 218 (Pubitemid 40385459)
3. E. Gabele, D.A. Brenner, and R.A. Rippe Liver fibrosis: signals leading to the amplification of the fibrogenic hepatic stellate cell Front Biosci 8 2003 D69 D77
4. M. Naito, G. Hasegawa, Y. Ebe, and T. Yamamoto Differentiation and function of Kupffer cells Med Electron Microsc 37 2004 16 28 (Pubitemid 38506718)
5. R.G. Thurman Alcoholic liver injury involves activation of Kupffer cells by endotoxin Am J Physiol 275 1998 G605 G611
6. A. Canbay, S. Friedman, and G.J. Gores Apoptosis: the nexus of liver injury and fibrosis Hepatology 39 2004 273 278 (Pubitemid 38222163)
7. S. Milani, H. Herbst, D. Schuppan, K.Y. Kim, E.O. Riecken, and H. Stein Procollagen expression by nonparenchymal rat liver cells in experimental biliary fibrosis Gastroenterology 98 1990 175 184 (Pubitemid 20017800)
8. O. Vias, R. Bataller, P. Sancho-Bru, P. Gins, C. Berenguer, C. Enrich, J.M. Nicolás, G. Ercilla, T. Gallart, J. Vives, V. Arroyo, and J. Rodés Human hepatic stellate cells show features of antigen-presenting cells and stimulate lymphocyte proliferation Hepatology 38 2003 919 929 (Pubitemid 37221675)
9. F. Marra Hepatic stellate cells and the regulation of liver inflammation J Hepatol 31 1999 1120 1130
10. J.J. Maher Interactions between hepatic stellate cells and the immune system Semin Liver Dis 21 2001 417 426 (Pubitemid 32923769)
11. M. Barczyk, S. Carracedo, and D. Gullberg Integrins Cell Tissue Res 339 2010 269 280
12. E. Olaso, K. Ikeda, F.J. Eng, L. Xu, L.H. Wang, H.C. Lin, and S.L. Friedman DDR2 receptor promotes MMP-2-mediated proliferation and invasion by hepatic stellate cells J Clin Invest 108 2001 1369 1378 (Pubitemid 33107765)
13. A. Shrivastava, C. Radziejewski, E. Campbell, L. Kovac, M. McGlynn, T.E. Ryan, S. Davis, M.P. Goldfarb, D.J. Glass, G. Lemke, and G.D. Yancopoulos An orphan receptor tyrosine kinase family whose members serve as nonintegrin collagen receptors Mol Cell 1 1997 25 34 (Pubitemid 127376390)
14. A.D. Konitsiotis, N. Raynal, D. Bihan, E. Hohenester, R.W. Farndale, and B. Leitinger Characterization of high affinity binding motifs for the discoidin domain receptor DDR2 in collagen Biol Chem 283 2008 6861 6868
15. L. Xu, J. Servais, I. Polur, D. Kim, P.L. Lee, K. Chung, and Y. Li Attenuation of osteoarthritis progression by reduction of discoidin domain receptor 2 in mice Arthritis Rheum 62 2010 2736 2744
16. T.K. Mao, Y. Kimura, T.P. Kenny, A. Branchi, R.G. Gishi, J. Van de Water, H.J. Kung, S.L. Friedman, and M.E. Gershwin Elevated expression of tyrosine kinase DDR2 in primary biliary cirrhosis Autoimmunity 35 2002 521 529 (Pubitemid 36321893)
17. X.H. Zhang, M. Yan, L. Liu, T.J. Wu, L.L. Ma, and L.X. Wang Expression of discoidin domain receptors (DDR2) in alcoholic liver fibrosis in rats Arch Med Res 41 2010 586 592
18. K. Ikeda, L.H. Wang, R. Torres, H. Zhao, E. Olaso, F.J. Eng, P. Labrador, R. Klein, D. Lovett, G.D. Yancopoulos, S.L. Friedman, and H.C. Lin Discoidin domain receptor 2 interacts with Src and Shc following its activation by type I collagen J Biol Chem 277 2002 19206 19212 (Pubitemid 34952488)
19. L.C. Junqueira, G. Bignolas, and R.R. Brentani Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections Histochem J 11 1979 447 455 (Pubitemid 9238595)
20. J.S. Duffield, S.J. Forbes, C.M. Constandinou, S. Clay, M. Partolina, S. Vuthoori, S. Wu, R. Lang, and J.P. Iredale Selective depletion of macrophages reveals distinct, opposing roles during liver injury and repair J Clin Invest 115 2005 56 65 (Pubitemid 40385505)
21. A. Sellers, E. Cartwright, G. Murphy, and J.J. Reynolds Evidence that latent collagenases are enzyme-inhibitor complexes Biochem J 163 1997 303 307
22. B. Hansen, B. Arteta, and B. Smedsrød The physiological scavenger receptor function of hepatic sinusoidal endothelial and Kupffer cells is independent of scavenger receptor class A type I and II Mol Cell Biochem 240 2002 1 8 (Pubitemid 35385815)
23. S. De Minicis, E. Seki, H. Uchinami, J. Klube, Y. Zhang, D.A. Brenner, and R.F. Schwabe Gene expression profiles during hepatic stellate cell activation in culture and in vivo Gastroenterology 132 2007 1937 1946 (Pubitemid 46677935)
24. M.J. Arthur Fibrogenesis II: metalloproteinases and their inhibitors in liver fibrosis Am J Physiol Gastrointest Liver Physiol 279 2000 G245 G249
25. P.A. Ruiz, and G. Jarai Collagen I induces discoidin domain receptor (DDR) 1 expression through DDR2 and a JAK2-ERK1/2-mediated mechanism in primary human lung fibroblasts J Biol Chem 286 2011 12912 12923
26. E. Olaso, H.C. Lin, L.H. Wang, and S.L. Friedman Impaired dermal wound healing in discoidin domain receptor 2-deficient mice associated with defective extracellular matrix remodeling Fibrogenesis Tissue Repair 4 2011 5
27. D.C. Rockey, J.K. Boyles, G. Gabbiani, and S.L. Friedman Rat hepatic lipocytes express smooth muscle actin upon activation in vivo and in culture J Submicrosc Cytol Pathol 24 1992 193 203
28. N. Ferré, M. Martínez-Clemente, M. López-Parra, A. González-Périz, R. Horrillo, A. Planagum, J. Camps, J. Joven, A. Tres, F. Guardiola, R. Bataller, V. Arroyo, and J. Clria Increased susceptibility to exacerbated liver injury in hypercholesterolemic ApoE-deficient mice: potential involvement of oxysterols Am J Physiol Gastrointest Liver Physiol 296 2009 G553 G562
29. J.A. Fallowfield, M. Mizuno, T.J. Kendall, C.M. Constandinou, R.C. Benyon, J.S. Duffield, and J.P. Iredale Scar-associated macrophages are a major source of hepatic matrix metalloproteinase-13 and facilitate the resolution of murine hepatic fibrosis J Immunol 178 2007 5288 5295 (Pubitemid 46595314)
30. S.W. Luckey, and D.R. Petersen Activation of Kupffer cells during the course of carbon tetrachloride-induced liver injury and fibrosis in rats Exp Mol Pathol 71 2001 226 240 (Pubitemid 34060097)
31. L. Xu, A.Y. Hui, E. Albanis, M.J. Arthur, S.M. O'Byrne, W.S. Blaner, P. Mukherjee, S.L. Friedman, and F.J. Eng Human hepatic stellate cell lines, LX-1 and LX-2: new tools for analysis of hepatic fibrosis Gut 54 2005 142 151 (Pubitemid 40007234)
32. T.A. Wynn, and L. Barron Macrophages: master regulators of inflammation and fibrosis Semin Liver Dis 30 2010 245 257
33. E. Faraci, M. Eckber, B. Gerstmayerc, A. Bosioc, and W.F. Vogel An extracellular matrix-specific microarray allowed the identification of target genes downstream of discoidin domain receptors Matrix Biol 22 2003 373 381 (Pubitemid 36993762)
34. J. Su, J. Yu, T. Ren, W. Zhang, Y. Zhang, X. Liu, T. Sun, H. Lu, K. Miyazawa, and L. Yao Discoidin domain receptor 2 is associated with the increased expression of matrix metalloproteinase-13 in synovial fibroblasts of rheumatoid arthritis Mol Cell Biochem 330 2009 141 152
35. N. Ferri, N.O. Carragher, and E.M. Raines Role of discoidin domain receptors 1 and 2 in human smooth muscle cell-mediated collagen remodeling: potential implications in atherosclerosis and lymphangioleiomyomatosis Am J Pathol 164 2004 1575 1585 (Pubitemid 38529760)
36. A.M. Gressner, R. Weiskirchen, K. Breitkopf, and S. Dooley Roles of TGF-beta in hepatic fibrosis Front Biosci 7 2002 d793-d780
37. R. Mori, T.J. Shaw, and P. Martin Molecular mechanisms linking wound inflammation and fibrosis: knockdown of osteopontin leads to rapid repair and reduced scarring J Exp Med 205 2008 43 51 (Pubitemid 351185714)
38. R. Kawashima, S. Mochida, A. Matsui, Y. YouLuTuZ, K. Ishikawa, K. Toshima, F. Yamanobe, M. Inao, H. Ikeda, A. Ohno, S. Nagoshi, T. Uede, and K. Fujiwara Expression of osteopontin in Kupffer cells and hepatic macrophages and stellate cells in rat liver after carbon tetrachloride intoxication: a possible factor for macrophage migration into hepatic necrotic areas Biochem Biophys Res Commun 256 1999 527 531 (Pubitemid 29301139)