Oval cell response is attenuated by depletion of liver resident macrophages in the 2-AAF/partial hepatectomy rat

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Xiang, Shuai ^a   Dong, Han Hua ^a   Liang, Hui Fang ^a   He, Song Qing ^b   Zhang, Wei ^b   Li, Chang Hai ^a   Zhang, Bi Xiang ^b   Zhang, Bin Hao ^b   Jing, Kai ^b   Tomlinson, Stephen ^c   van Rooijen, Nico ^d   Jiang, Li ^a   Cianflone, Katherine ^e   Chen, Xiao Ping ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b GUILIN MEDICAL UNIVERSITY   (China)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^d VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^e LAVAL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; AMINOTRANSFERASE; CLODRONIC ACID; CYTOKERATIN; EPITHELIAL CELL ADHESION MOLECULE; INTERLEUKIN 6; LIPOSOME; MESSENGER RNA; N (2 FLUORENYL)ACETAMIDE; PANCYTOKERATIN; STAT3 PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL EXPANSION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; LIVER CELL; LIVER INJURY; LIVER PARENCHYMA; LIVER REGENERATION; LIVER TUMOR; MACROPHAGE; MACROPHAGE DEPLETION; MACROPHAGE FUNCTION; MALE; MORTALITY; NONHUMAN; OVAL CELL; PARTIAL HEPATECTOMY; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; RAT; REAL TIME POLYMERASE CHAIN REACTION; STEM CELL; ANIMAL; CELL LINE; CYTOLOGY; DRUG EFFECT; LIVER RESECTION; METABOLISM; NICK END LABELING; WESTERN BLOTTING;

RATTUS;

2-ACETYLAMINOFLUORENE; ANIMALS; BLOTTING, WESTERN; CELL LINE; HEPATECTOMY; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; LIPOSOMES; LIVER REGENERATION; MACROPHAGES; RATS; REAL-TIME POLYMERASE CHAIN REACTION; STEM CELLS;

EID: 84859706006     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035180     Document Type: Article

References (48)

1. Roskams TA, Libbrecht L, Desmet VJ, (2003) Progenitor cells in diseased human liver. Semin Liver Dis 23: 385-396.
2. Kuhlmann WD, Peschke P, (2006) Hepatic progenitor cells, stem cells, and AFP expression in models of liver injury. Int J Exp Pathol 87: 343-359.
3. Libbrecht L, Roskams T, (2002) Hepatic progenitor cells in human liver diseases. Semin Cell Dev Biol 13: 389-396.
4. Santoni-Rugiu E, Jelnes P, Thorgeirsson SS, Bisgaard HC, (2005) Progenitor cells in liver regeneration: molecular responses controlling their activation and expansion. Apmis 113: 876-902.
5. Shupe T, Petersen BE, (2005) Evidence regarding a stem cell origin of hepatocellular carcinoma. Stem Cell Rev 1: 261-264.
6. Lee JS, Heo J, Libbrecht L, Chu IS, Kaposi-Novak P, et al. (2006) A novel prognostic subtype of human hepatocellular carcinoma derived from hepatic progenitor cells. Nat Med 12: 410-416.
7. Braun L, Mikumo R, Fausto N, (1989) Production of hepatocellular carcinoma by oval cells: cell cycle expression of c-myc and p53 at different stages of oval cell transformation. Cancer Res 49: 1554-1561.
8. Theise ND, (2006) Gastrointestinal stem cells. III. Emergent themes of liver stem cell biology: niche, quiescence, self-renewal, and plasticity. Am J Physiol Gastrointest Liver Physiol 290: G189-193.
9. Strick-Marchand H, Masse GX, Weiss MC, Di Santo JP, (2008) Lymphocytes support oval cell-dependent liver regeneration. J Immunol 181: 2764-2771.
10. Knight B, Akhurst B, Matthews VB, Ruddell RG, Ramm GA, et al. (2007) Attenuated liver progenitor (oval) cell and fibrogenic responses to the choline deficient, ethionine supplemented diet in the BALB/c inbred strain of mice. J Hepatol 46: 134-141.
11. Lowes KN, Brennan BA, Yeoh GC, Olynyk JK, (1999) Oval cell numbers in human chronic liver diseases are directly related to disease severity. Am J Pathol 154: 537-541.
12. Libbrecht L, Desmet V, van Damme B, Roskams T, (2000) The immunohistochemical phenotype of dysplastic foci in human liver: correlation with putative progenitor cells. J Hepatol 33: 76-84.
13. Abshagen K, Eipel C, Kalff JC, Menger MD, Vollmar B, (2007) Loss of NF-kappaB activation in Kupffer cell-depleted mice impairs liver regeneration after partial hepatectomy. Am J Physiol Gastrointest Liver Physiol 292: G1570-1577.
14. Meijer C, Wiezer MJ, Diehl AM, Yang S-Q, Schouten HJ, et al. (2000) Kupffer cell depletion by CI2MDP-liposomes alters hepatic cytokine expression and delays liver regeneration after partial hepatectomy. Liver 20: 66-77.
15. Boulton RA, Alison MR, Golding M, Selden C, Hodgson HJ, (1998) Augmentation of the early phase of liver regeneration after 70% partial hepatectomy in rats following selective Kupffer cell depletion. J Hepatol 29: 271-280.
16. Rai RM, Yang SQ, McClain C, Karp CL, Klein AS, et al. (1996) Kupffer cell depletion by gadolinium chloride enhances liver regeneration after partial hepatectomy in rats. Am J Physiol 270: G909-918.
17. Zhang W, Chen XP, Zhang WG, Zhang F, Xiang S, et al. (2009) Hepatic non-parenchymal cells and extracellular matrix participate in oval cell-mediated liver regeneration. World J Gastroenterol 15: 552-560.
18. Yin L, Lynch D, Ilic Z, Sell S, (2002) Proliferation and differentiation of ductular progenitor cells and littoral cells during the regeneration of the rat liver to CCl4/2-AAF injury. Histol Histopathol 17: 65-81.
19. Decker K, (1990) Biologically active products of stimulated liver macrophages (Kupffer cells). Eur J Biochem 192: 245-261.
20. Olynyk JK, Yeoh GC, Ramm GA, Clarke SL, Hall PM, et al. (1998) Gadolinium chloride suppresses hepatic oval cell proliferation in rats with biliary obstruction. Am J Pathol 152: 347-352.
21. Paku S, Schnur J, Nagy P, Thorgeirsson SS, (2001) Origin and structural evolution of the early proliferating oval cells in rat liver. Am J Pathol 158: 1313-1323.
22. Jensen CH, Jauho EI, Santoni-Rugiu E, Holmskov U, Teisner B, et al. (2004) 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 164: 1347-1359.
23. Faa G, van Eyken P, Roskams T, Miyazaki H, Serreli S, et al. (1998) Expression of cytokeratin 20 in developing rat liver and in experimental models of ductular and oval cell proliferation. J Hepatol 29: 628-633.
24. Nagy P, Kiss A, Schnur J, Thorgeirsson SS, (1998) Dexamethasone inhibits the proliferation of hepatocytes and oval cells but not bile duct cells in rat liver. Hepatology 28: 423-429.
25. Devey L, Ferenbach D, Mohr E, Sangster K, Bellamy CO, et al. (2009) Tissue-resident macrophages protect the liver from ischemia reperfusion injury via a heme oxygenase-1-dependent mechanism. Mol Ther 17: 65-72.
26. Hardonk MJ, Dijkhuis FW, Hulstaert CE, Koudstaal J, (1992) Heterogeneity of rat liver and spleen macrophages in gadolinium chloride-induced elimination and repopulation. J Leukoc Biol 52: 296-302.
27. van Rooijen N, Sanders A, (1996) Kupffer cell depletion by liposome-delivered drugs: comparative activity of intracellular clodronate, propamidine, and ethylenediaminetetraacetic acid. Hepatology 23: 1239-1243.
28. van Rooijen N, Sanders A, (1994) Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J Immunol Methods 174: 83-93.
29. van Rooijen N, Kors N, vd Ende M, Dijkstra CD, (1990) Depletion and repopulation of macrophages in spleen and liver of rat after intravenous treatment with liposome-encapsulated dichloromethylene diphosphonate. Cell Tissue Res 260: 215-222.
30. Laszlo V, Dezso K, Baghy K, Papp V, Kovalszky I, et al. (2008) Triiodothyronine accelerates differentiation of rat liver progenitor cells into hepatocytes. Histochem Cell Biol 130: 1005-1014.
31. Evarts RP, Hu Z, Omori N, Omori M, Marsden ER, et al. (1996) Precursor-product relationship between oval cells and hepatocytes: comparison between tritiated thymidine and bromodeoxyuridine as tracers. Carcinogenesis 17: 2143-2151.
32. Evarts RP, Nagy P, Marsden E, Thorgeirsson SS, (1987) A precursor-product relationship exists between oval cells and hepatocytes in rat liver. Carcinogenesis 8: 1737-1740.
33. Lowes KN, Croager EJ, Olynyk JK, Abraham LJ, Yeoh GC, (2003) Oval cell-mediated liver regeneration: Role of cytokines and growth factors. J Gastroenterol Hepatol 18: 4-12.
34. Gao B, (2005) Cytokines, STATs and liver disease. Cell Mol Immunol 2: 92-100.
35. Fausto N, Campbell JS, Riehle KJ, (2006) Liver regeneration. Hepatology 43: S45-53.
36. Lee CM, Yeoh GC, Olynyk JK, (2004) Differential effects of gadolinium chloride on Kupffer cells in vivo and in vitro. Int J Biochem Cell Biol 36: 481-488.
37. Ju C, Reilly TP, Bourdi M, Radonovich MF, Brady JN, et al. (2002) Protective role of Kupffer cells in acetaminophen-induced hepatic injury in mice. Chem Res Toxicol 15: 1504-1513.
38. Gregory SH, Wing EJ, Danowski KL, van Rooijen N, Dyer KF, et al. (1998) IL-6 produced by Kupffer cells induces STAT protein activation in hepatocytes early during the course of systemic listerial infections. J Immunol 160: 6056-6061.
39. Fausto N, Campbell JS, (2003) The role of hepatocytes and oval cells in liver regeneration and repopulation. Mech Dev 120: 117-130.
40. Dong ZJ, Wei HM, Sun R, Tian ZG, (2007) The roles of innate immune cells in liver injury and regeneration. Cell Mol Immunol 4: 241-252.
41. Bilzer M, Roggel F, Gerbes AL, (2006) Role of Kupffer cells in host defense and liver disease. Liver Int 26: 1175-1186.
42. Knight B, Yeoh GC, Husk KL, Ly T, Abraham LJ, et al. (2000) Impaired preneoplastic changes and liver tumor formation in tumor necrosis factor receptor type 1 knockout mice. J Exp Med 192: 1809-1818.
43. Jin C, Samuelson L, Cui CB, Sun Y, Gerber DA, (2011) MAPK/ERK and Wnt/beta-Catenin pathways are synergistically involved in proliferation of Sca-1 positive hepatic progenitor cells. Biochem Biophys Res Commun 409: 803-807.
44. Dong X, Zhao H, Ma X, Wang S, (2010) Reduction in bile acid pool causes delayed liver regeneration accompanied by down-regulated expression of FXR and c-Jun mRNA in rats. J Huazhong Univ Sci Technolog Med Sci 30: 55-60.
45. Viebahn CS, Benseler V, Holz LE, Elsegood CL, Vo M, et al. (2010) Invading macrophages play a major role in the liver progenitor cell response to chronic liver injury. J Hepatol 53: 500-507.
46. Kinoshita M, Uchida T, Sato A, Nakashima M, Nakashima H, et al. (2010) Characterization of two F4/80-positive Kupffer cell subsets by their function and phenotype in mice. J Hepatol 53: 903-910.
47. Nagy P, Bisgaard HC, Thorgeirsson SS, (1994) Expression of hepatic transcription factors during liver development and oval cell differentiation. J Cell Biol 126: 223-233.
48. Evarts RP, Nagy P, Nakatsukasa H, Marsden E, Thorgeirsson SS, (1989) In vivo differentiation of rat liver oval cells into hepatocytes. Cancer Res 49: 1541-1547.