Molecular constituents of the extracellular matrix in rat liver mounting a hepatic progenitor cell response for tissue repair
详细信息 查看全文
- 作者：Peter Siig Vestentoft (1)
Peter Jelnes (1)
Jesper B Andersen (2)
Thi Anh Thu Tran (1)
Tenna J?rgensen (1)
Morten Rasmussen (1) (3)
Jette Bornholdt (1)
Lene Mels?ther Gr?vdal (1)
Charlotte Harken Jensen (4) (5)
Lotte Katrine Vogel (1)
Snorri S Thorgeirsson (2)
Hanne Cathrine Bisgaard (1) - 关键词：Ductular reaction ; Extracellular matrix constituents ; First and second tiers of defense ; Hepatic progenitor (oval) cell reaction ; Liver injury and repair ; Three ; dimensional reconstruction
- 刊名：Fibrogenesis & Tissue Repair
- 出版年：2013
- 出版时间：December 2013
- 年：2013
- 卷：6
- 期：1
- 全文大小：1,967 KB
- 参考文献：1. Riehle KJ, Dan YY, Campbell JS, Fausto N: New concepts in liver regeneration. / J Gastroenterol Hepatol 2011,26(Suppl 1):203-12. CrossRef
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, 158:1313-323. CrossRef
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, 39:1353-361. CrossRef
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, 30:1425-433. CrossRef
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, 47:1994-002. CrossRef
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, 59:645-54. CrossRef
7. Fuchs E, Tumbar T, Guasch G: Socializing with the neighbors: stem cells and their niche. / Cell 2004, 116:769-78. CrossRef
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, 21:159-71. CrossRef
9. Santoni-Rugiu E, Jelnes P, Thorgeirsson SS, Bisgaard HC: Progenitor cells in liver regeneration: molecular responses controlling their activation and expansion. / APMIS 2005, 113:876-02. CrossRef
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, 128:2077-088. CrossRef
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, 47:996-004. CrossRef
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, 45:31-1. CrossRef
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, 27:674-81. CrossRef
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, 55:1965-975. CrossRef
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, 49:1625-635. CrossRef
16. Duncan AW, Dorrell C, Grompe M: Stem cells and liver regeneration. / Gastroenterology 2009, 137:466-81. CrossRef
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, 45:1462-470. CrossRef
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, 164:1347-359. CrossRef
19. Vestentoft PS, Jelnes P, Hopkinson BM, Vainer B, M?llg?rd K, Quistorff B, Bisgaard HC: Three-dimensional reconstructions of intrahepatic bile duct tubulogenesis in human liver. / BMC Dev Biol 2011, 11:56. CrossRef
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, 47:636-47. CrossRef
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, 275:36720-6725. CrossRef
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, 288:19028-9039. CrossRef
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, 285:31755-1762. CrossRef
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, 283:29495-9504. CrossRef
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, 319:918-29. CrossRef
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, 5:209-18. CrossRef
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, 90:1199-208. CrossRef
28. Dezso K, Jelnes P, László V, Baghy K, B?d?r 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, 171:1529-537. CrossRef
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, 60:525-33. CrossRef
30. Daley WP, Peters SB, Larsen M: Extracellular matrix dynamics in development and regenerative medicine. / J Cell Sci 2008, 121:255-64. CrossRef
31. van der Flier A, Sonnenberg A: Function and interactions of integrins. / Cell Tissue Res 2001, 305:285-98. CrossRef
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, 25:1474-485. CrossRef
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, 125:611-19.
34. Rojkind M, Giambrone MA, Biempica L: Collagen types in normal and cirrhotic liver. / Gastroenterology 1979, 76:710-19.
35. Ho MS, Bose K, Mokkapati S, Nischt R, Smyth N: Nidogens - extracellular matrix linker molecules. / Microsc Res Tech 2008, 71:387-95. CrossRef
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, 86:1149-160.
37. Bezakova G, Ruegg MA: New insights into the roles of agrin. / Nat Rev Mol Cell Biol 2003, 4:295-08. CrossRef
38. Clayton E, Forbes SJ: The isolation and in vitro expansion of hepatic Sca-1 progenitor cells. / Biochem Biophys Res Commun 2009, 381:549-53. CrossRef
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, 14:59-0. CrossRef
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, 287:28586-8597. CrossRef
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, 47:673-82. CrossRef
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, 55:161-72. CrossRef
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, 155:1075-085. CrossRef
44. Bustin SA: Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. / J Mol Endocrinol 2000, 25:169-93. CrossRef - 作者单位：Peter Siig Vestentoft (1)
Peter Jelnes (1)
Jesper B Andersen (2)
Thi Anh Thu Tran (1)
Tenna J?rgensen (1)
Morten Rasmussen (1) (3)
Jette Bornholdt (1)
Lene Mels?ther Gr?vdal (1)
Charlotte Harken Jensen (4) (5)
Lotte Katrine Vogel (1)
Snorri S Thorgeirsson (2)
Hanne Cathrine Bisgaard (1)
1. Department of Cellular and Molecular Medicine, Faculty of Health and Medical Sciences, University of Copenhagen, Blegdamsvej 3, DK, 2200, Copenhagen, Denmark
2. Laboratory of Experimental Carcinogenesis, National Cancer Institute, National Institutes of Health, Bethesda, MD, USA
3. The Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health Sciences, University of Copenhagen, Copenhagen, Denmark
4. Laboratory of Molecular and Cellular Cardiology, Department of Clinical Biochemistry and Pharmacology, Odense University Hospital, Odense, Denmark
5. Department of Cardiovascular and Renal Research, University of Southern Denmark, Odense, Denmark - ISSN：1755-1536
文摘
Background Tissue repair in the adult mammalian liver occurs in two distinct processes, referred to as the first and second tiers of defense. We undertook to characterize the changes in molecular constituents of the extracellular matrix when hepatic progenitor cells (HPCs) respond in a second tier of defense to liver injury. Results We used transcriptional profiling on rat livers responding by a first tier (surgical removal of 70% of the liver mass (PHx protocol)) and a second tier (70% hepatectomy combined with exposure to 2-acetylaminofluorene (AAF/PHx protocol)) of defense to liver injury and compared the transcriptional signatures in untreated rat liver (control) with those from livers of day 1, day 5 and day 9 post hepatectomy in both protocols. Numerous transcripts encoding specific subunits of collagens, laminins, integrins, and various other extracellular matrix structural components were differentially up- or down-modulated (P-lt;-.01). The levels of a number of transcripts were significantly up-modulated, mainly in the second tier of defense (Agrn, Bgn, Fbn1, Col4a1, Col8a1, Col9a3, Lama5, Lamb1, Lamb2, Itga4, Igtb2, Itgb4, Itgb6, Nid2), and their signal intensities showed a strong or very strong correlation with Krt1-19, a well-established marker of a ductular/HPC reaction. Furthermore, a significant up-modulation and very strong correlation between the transcriptional profiles of Krt1-19 and St14 encoding matriptase, a component of a novel protease system, was found in the second tier of defense. Real-time PCR confirmed the modulation of St14 transcript levels and strong correlation to Krt-19 and also showed a significant up-modulation and strong correlation to Spint1 encoding HAI-1, a cognate inhibitor of matriptase. Immunodetection and three-dimensional reconstructions showed that laminin, Collagen1a1, agrin and nidogen1 surrounded bile ducts, proliferating cholangiocytes, and HPCs in ductular reactions regardless of the nature of defense. Similarly, matriptase and HAI-1 were expressed in cholangiocytes regardless of the tier of defense, but in the second tier of defense, a subpopulation of HPCs in ductular reactions co-expressed HAI-1 and the fetal hepatocyte marker Dlk1. Conclusion Transcriptional profiling and immunodetection, including three-dimensional reconstruction, generated a detailed overview of the extracellular matrix constituents expressed in a second tier of defense to liver injury.