Molecular constituents of the extracellular matrix in rat liver mounting a hepatic progenitor cell response for tissue repair

Fibrogenesis and Tissue Repair

Volumn 6, Issue 1, 2013, Pages

  Vestentoft, Peter S ^a   Jelnes, Peter ^a   Andersen, Jesper B ^b   Tran, Thi Anh T ^a   Jørgensen, Tenna ^a   Rasmussen, Morten ^a,c   Bornholdt, Jette ^a   Grøvdal, Lene M ^a   Jensen, Charlotte H ^d,e   Vogel, Lotte K ^a   Thorgeirsson, Snorri S ^b   Bisgaard, Hanne C ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b NATIONAL CANCER INSTITUTE   (United States)

^c Capital Region   (Denmark)

^d ODENSE UNIVERSITY HOSPITAL   (Denmark)

^e UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Ductular reaction; Extracellular matrix constituents; First and second tiers of defense; Hepatic progenitor (oval) cell reaction; Liver injury and repair; Three dimensional reconstruction

Indexed keywords

AGRIN; ALPHA FETOPROTEIN; BIGLYCAN; CALVASCULIN; CD133 ANTIGEN; CD24 ANTIGEN; COLLAGEN; CONNECTIVE TISSUE GROWTH FACTOR; CONNEXIN 43; CYCLINE; CYTOKERATIN 19; DECORIN; DESMIN; ELASTIN; ENTACTIN; EPITHELIAL CELL ADHESION MOLECULE; FIBRILLIN 1; FIBULIN; GLUTATHIONE TRANSFERASE P1; GLYPICAN 3; INTEGRIN; LAMININ; MATRIPTASE; MATRIX METALLOPROTEINASE; N (2 FLUORENYL)ACETAMIDE; OSTEONECTIN; OSTEOPONTIN; PROTEINASE; SYNDECAN; VIMENTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILE DUCT; CELL SUBPOPULATION; COL4A1 GENE; COL8A1 GENE; COL9A3 GENE; CONTROLLED STUDY; EPITHELIUM CELL; EXTRACELLULAR MATRIX; GENE; GENETIC TRANSCRIPTION; HEPATIC PROGENITOR CELL; IMAGE RECONSTRUCTION; IMMUNODETECTION; ITGA4 GENE; ITGB4 GENE; ITGB6 GENE; LAMA5 GENE; LAMB1 GENE; LAMB2 GENE; LIVER; LIVER HISTOLOGY; LIVER INJURY; LIVER RESECTION; MALE; NID2 GENE; NONHUMAN; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; STEM CELL; THREE DIMENSIONAL IMAGING; TISSUE REPAIR;

EID: 84890513630     PISSN: None     EISSN: 17551536     Source Type: Journal    
DOI: 10.1186/1755-1536-6-21     Document Type: Article

References (44)

1. Riehle KJ, Dan YY, Campbell JS, Fausto N. New concepts in liver regeneration. J Gastroenterol Hepatol 2011, 26(Suppl 1):203-212. 3077908, 21199532.
2. Paku S, Schnur J, Nagy P, Thorgeirsson SS. Origin and structural evolution of the early proliferating oval cells in rat liver. Am J Pathol 2001, 158:1313-1323. 10.1016/S0002-9440(10)64082-5, 1891899, 11290549.
3. Paku S, Nagy P, Kopper L, Thorgeirsson SS. 2-acetylaminofluorene dose-dependent differentiation of rat oval cells into hepatocytes: confocal and electron microscopic studies. Hepatology 2004, 39:1353-1361. 10.1002/hep.20178, 15122764.
4. Theise ND, Saxena R, Portmann BC, Thung SN, Yee H, Chiriboga L, Kumar A, Crawford JM. The canals of Hering and hepatic stem cells in humans. Hepatology 1999, 30:1425-1433. 10.1002/hep.510300614, 10573521.
5. Kuwahara R, Kofman AV, Landis CS, Swenson ES, Barendswaard E, Theise ND. The hepatic stem cell niche: identification by label-retaining cell assay. Hepatology 2008, 47:1994-2002. 10.1002/hep.22218, 2847183, 18454509.
6. Lorenzini S, Bird TG, Boulter L, Bellamy C, Samuel K, Aucott R, Clayton E, Andreone P, Bernardi M, Golding M, Alison MR, Iredale JP, Forbes SJ. Characterisation of a stereotypical cellular and extracellular adult liver progenitor cell niche in rodents and diseased human liver. Gut 2010, 59:645-654. 10.1136/gut.2009.182345, 3034133, 20427399.
7. Fuchs E, Tumbar T, Guasch G. Socializing with the neighbors: stem cells and their niche. Cell 2004, 116:769-778. 10.1016/S0092-8674(04)00255-7, 15035980.
8. Losick VP, Morris LX, Fox DT, Spradling A. Drosophila stem cell niches: a decade of discovery suggests a unified view of stem cell regulation. Dev Cell 2011, 21:159-171. 10.1016/j.devcel.2011.06.018, 21763616.
9. Santoni-Rugiu E, Jelnes P, Thorgeirsson SS, Bisgaard HC. Progenitor cells in liver regeneration: molecular responses controlling their activation and expansion. APMIS 2005, 113:876-902. 10.1111/j.1600-0463.2005.apm_386.x, 16480456.
10. Pi L, Oh SH, Shupe T, Petersen BE. Role of connective tissue growth factor in oval cell response during liver regeneration after 2-AAF/PHx in rats. Gastroenterology 2005, 128:2077-2088. 10.1053/j.gastro.2005.03.081, 3756499, 15940639.
11. Pi L, Ding X, Jorgensen M, Pan JJ, Oh SH, Pintilie D, Brown A, Song WY, Petersen BE. Connective tissue growth factor with a novel fibronectin binding site promotes cell adhesion and migration during rat oval cell activation. Hepatology 2008, 47:996-1004. 10.1002/hep.22079, 3130595, 18167060.
12. Nguyen LN, Furuya MH, Wolfraim LA, Nguyen AP, Holdren MS, Campbell JS, Knight B, Yeoh GC, Fausto N, Parks WT. Transforming growth factor-β differentially regulates oval cell and hepatocyte proliferation. Hepatology 2007, 45:31-41. 10.1002/hep.21466, 17187411.
13. Pham VT, Couchie D, Martin-Garcia N, Laperche Y, Zafrani ES, Mavier P. Expression of matrix metalloproteinase-2 and -9 and of tissue inhibitor of matrix metalloproteinase-1 in liver regeneration from oval cells in rat. Matrix Biol 2008, 27:674-681. 10.1016/j.matbio.2008.07.002, 18678246.
14. Pellicoro A, Aucott RL, Ramachandran P, Robson AJ, Fallowfield JA, Snowdon VK, Hartland SN, Vernon M, Duffield JS, Benyon RC, Forbes SJ, Iredale JP. Elastin accumulation is regulated at the level of degradation by macrophage metalloelastase (MMP-12) during experimental liver fibrosis. Hepatology 2012, 55:1965-1975. 10.1002/hep.25567, 22223197.
15. Van Hul NK, Abarca-Quinones J, Sempoux C, Horsmans Y, Leclercq IA. Relation between liver progenitor cell expansion and extracellular matrix deposition in a CDE-induced murine model of chronic liver injury. Hepatology 2009, 49:1625-1635. 10.1002/hep.22820, 19296469.
16. Duncan AW, Dorrell C, Grompe M. Stem cells and liver regeneration. Gastroenterology 2009, 137:466-481. 10.1053/j.gastro.2009.05.044, 3136245, 19470389.
17. Jelnes P, Santoni-Rugiu E, Rasmussen M, Friis SL, Nielsen JH, Tygstrup N, Bisgaard HC. Remarkable heterogeneity displayed by oval cells in rat and mouse models of stem cell-mediated liver regeneration. Hepatology 2007, 45:1462-1470. 10.1002/hep.21569, 17538966.
18. Jensen CH, Jauho EI, Santoni-Rugiu E, Holmskov U, Teisner B, Tygstrup N, Bisgaard HC. Transit-amplifying ductular (oval) cells and their hepatocytic progeny are characterized by a novel and distinctive expression of delta-like protein/preadipocyte factor 1/fetal antigen 1. Am J Pathol 2004, 164:1347-1359. 10.1016/S0002-9440(10)63221-X, 1615354, 15039222.
19. Vestentoft PS, Jelnes P, Hopkinson BM, Vainer B, Møllgård K, Quistorff B, Bisgaard HC. Three-dimensional reconstructions of intrahepatic bile duct tubulogenesis in human liver. BMC Dev Biol 2011, 11:56. 10.1186/1471-213X-11-56, 3192761, 21943389.
20. Yovchev MI, Grozdanov PN, Zhou H, Racherla H, Guha C, Dabeva MD. Identification of adult hepatic progenitor cells capable of repopulating injured rat liver. Hepatology 2008, 47:636-647.
21. Lee SL, Dickson RB, Lin CY. Activation of hepatocyte growth factor and urokinase/plasminogen activator by matriptase, an epithelial membrane serine protease. J Biol Chem 2000, 275:36720-36725. 10.1074/jbc.M007802200, 10962009.
22. Friis S, Uzzun Sales K, Godiksen S, Peters DE, Lin CY, Vogel LK, Bugge TH. A matriptase-prostasin reciprocal zymogen activation complex with unique features: prostasin as a non-enzymatic co-factor for matriptase activation. J Biol Chem 2013, 288:19028-19039. 10.1074/jbc.M113.469932, 23673661.
23. Chen YW, Wang JK, Chou FP, Chen CY, Rorke EA, Chen LM, Chai KX, Eckert RL, Johnson MD, Lin CY. Regulation of the matriptase-prostasin cell surface proteolytic cascade by hepatocyte growth factor activator inhibitor-1 during epidermal differentiation. J Biol Chem 2010, 285:31755-31762. 10.1074/jbc.M110.150367, 2951247, 20696767.
24. Szabo R, Hobson JP, List K, Molinolo A, Lin CY, Bugge TH. Potent inhibition and global co-localization implicate the transmembrane Kunitz-type serine protease inhibitor hepatocyte growth factor activator inhibitor-2 in the regulation of epithelial matriptase activity. J Biol Chem 2008, 283:29495-29504. 10.1074/jbc.M801970200, 2570866, 18713750.
25. Larsen BR, Steffensen SD, Nielsen NV, Friis S, Godiksen S, Bornholdt J, Soendergaard C, Nonboe AW, Andersen MN, Poulsen SS, Szabo R, Bugge TH, Lin CY, Skovbjerg H, Jensen JK, Vogel LK. Hepatocyte growth factor activator inhibitor-2 prevents shedding of matriptase. Exp Cell Res 2013, 319:918-929. 10.1016/j.yexcr.2013.01.008, 23333561.
26. Tanimizu N, Tsujimura T, Takahide K, Kodama T, Nakamura K, Miyajima A. Expression of Dlk/Pref-1 defines a subpopulation in the oval cell compartment of rat liver. Gene Expr Patterns 2004, 5:209-218. 10.1016/j.modgep.2004.08.003, 15567716.
27. Pintilie DG, Shupe TD, Oh SH, Salganik SV, Darwiche H, Petersen BE. Hepatic stellate cells' involvement in progenitor-mediated liver regeneration. Lab Invest 2010, 90:1199-1208. 10.1038/labinvest.2010.88, 2912420, 20440274.
28. Dezso K, Jelnes P, László V, Baghy K, Bödör C, Paku S, Tygstrup N, Bisgaard HC, Nagy P. Thy-1 is expressed in hepatic myofibroblasts and not oval cells in stem cell-mediated liver regeneration. Am J Pathol 2007, 171:1529-1537. 10.2353/ajpath.2007.070273, 2043514, 17884967.
29. Kallis YN, Robson AJ, Fallowfield JA, Thomas HC, Alison MR, Wright NA, Goldin RD, Iredale JP, Forbes SJ. Remodelling of extracellular matrix is a requirement for the hepatic progenitor cell response. Gut 2011, 60:525-533. 10.1136/gut.2010.224436, 21106552.
30. Daley WP, Peters SB, Larsen M. Extracellular matrix dynamics in development and regenerative medicine. J Cell Sci 2008, 121:255-264. 10.1242/jcs.006064, 18216330.
31. van der Flier A, Sonnenberg A. Function and interactions of integrins. Cell Tissue Res 2001, 305:285-298. 10.1007/s004410100417, 11572082.
32. Sun Y, Li W, Lu Z, Chen R, Ling J, Ran Q, Jilka RL, Chen XD. Rescuing replication and osteogenesis of aged mesenchymal stem cells by exposure to a young extracellular matrix. FASEB J 2011, 25:1474-1485. 10.1096/fj.10-161497, 3079301, 21248241.
33. Ogawa K, Suzuki J, Mukai H, Mori M. Sequential changes of extracellular matrix and proliferation of Ito cells with enhanced expression of desmin and actin in focal hepatic injury. Am J Pathol 1986, 125:611-619. 1888465, 3799820.
34. Rojkind M, Giambrone MA, Biempica L. Collagen types in normal and cirrhotic liver. Gastroenterology 1979, 76:710-719.
35. Ho MS, Bose K, Mokkapati S, Nischt R, Smyth N. Nidogens - extracellular matrix linker molecules. Microsc Res Tech 2008, 71:387-395. 10.1002/jemt.20567, 18219668.
36. Tátrai P, Dudás J, Batmunkh E, Máthé M, Zalatnai A, Schaff Z, Ramadori G, Kovalszky I. Agrin, a novel basement membrane component in human and rat liver, accumulates in cirrhosis and hepatocellular carcinoma. Lab Invest 2006, 86:1149-1160.
37. Bezakova G, Ruegg MA. New insights into the roles of agrin. Nat Rev Mol Cell Biol 2003, 4:295-308. 10.1038/nrm1074, 12671652.
38. Clayton E, Forbes SJ. The isolation and in vitro expansion of hepatic Sca-1 progenitor cells. Biochem Biophys Res Commun 2009, 381:549-553. 10.1016/j.bbrc.2009.02.079, 19233130.
39. McClelland R, Wauthier E, Uronis J, Reid L. Gradients in the liver's extracellular matrix chemistry from periportal to pericentral zones: influence on human hepatic progenitors. Tissue Eng Part A 2008, 14:59-70. 10.1089/ten.a.2007.0058, 18333805.
40. Tanimizu N, Kikkawa Y, Mitaka T, Miyajima A. α1- and α5-containing laminins regulate the development of bile ducts via β1-integrin signals. J Biol Chem 2012, 287:28586-28597. 10.1074/jbc.M112.350488, 3436529, 22761447.
41. Kataoka H, Suganuma T, Shimomura T, Itoh H, Kitamura N, Nabeshima K, Koono M. Distribution of hepatocyte growth factor activator inhibitor type 1 (HAI-1) in human tissues. Cellular surface localization of HAI-1 in simple columnar epithelium and its modulated expression in injured and regenerative tissues. J Histochem Cytochem 1999, 47:673-682. 10.1177/002215549904700509, 10219059.
42. Huang HP, Chang MH, Chen YT, Hsu HY, Chiang CL, Cheng TS, Wu YM, Wu MZ, Hsu YC, Shen CC, Lee CN, Chuang YH, Hong CL, Jeng YM, Chen PH, Chen HL, Lee MS. Persistent elevation of hepatocyte growth factor activator inhibitors in cholangiopathies affects liver fibrosis and differentiation. Hepatology 2012, 55:161-172. 10.1002/hep.24657, 21898507.
43. Bisgaard HC, Muller S, Nagy P, Rasmussen LJ, Thorgeirsson SS. Modulation of the gene network connected to interferon-gamma in liver regeneration from oval cells. Am J Pathol 1999, 155:1075-1085. 10.1016/S0002-9440(10)65210-8, 1867006, 10514390.
44. Bustin SA. Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J Mol Endocrinol 2000, 25:169-193. 10.1677/jme.0.0250169, 11013345.