Origin of myofibroblasts in the fibrotic liver in mice

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 32, 2014, Pages

  Iwaisako, Keiko ^a,b   Jiang, Chunyan ^a,c   Zhang, Mingjun ^a   Cong, Min ^a,c   Moore Morris, Thomas Joseph ^a   Park, Tae Jun ^a   Liu, Xiao ^a   Xu, Jun ^a   Wang, Ping ^a,c   Paik, Yong Han ^d   Meng, Fanli ^a,e   Asagiri, Masataka ^b   Murray, Lynne A ^f   Hofmann, Alan F ^a   Iida, Takashi ^g   Glass, Christopher K ^a   Brenner, David A ^a   Kisseleva, Tatiana ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b KYOTO UNIVERSITY   (Japan)

^c CAPITAL MEDICAL UNIVERSITY   (China)

^d Sungkyunkwan University School of Medicine   (South Korea)

^e SHANDONG UNIVERSITY   (China)

^f MEDIMMUNE   (United States)

^g NIHON UNIVERSITY   (Japan)

Author keywords

ECM deposition; Markers of fibrogenic myofibroblasts

Indexed keywords

CARBON TETRACHLORIDE; COLLAGEN; COLLAGEN TYPE 1; INTERLEUKIN 13; INTERLEUKIN 25; TAUROCHOLIC ACID;

ANIMAL CELL; ARTICLE; BILE DUCT LIGATION; CELL ACTIVATION; CELL POPULATION; CHOLESTASIS; CONTROLLED STUDY; FIBROBLAST; FLOW CYTOMETRY; GENE EXPRESSION; LIVER FIBROSIS; LIVER INJURY; LIVER TOXICITY; MOUSE; MYOFIBROBLAST; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; STELLATE CELL; STIMULATION;

ECM DEPOSITION; MARKERS OF FIBROGENIC MYOFIBROBLASTS;

ANIMALS; CARBON TETRACHLORIDE; CHOLESTASIS; COLLAGEN TYPE I; DISEASE MODELS, ANIMAL; DRUG-INDUCED LIVER INJURY; GPI-LINKED PROTEINS; GREEN FLUORESCENT PROTEINS; HEPATIC STELLATE CELLS; LIVER; LIVER CIRRHOSIS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYOFIBROBLASTS; RECOMBINANT PROTEINS; VITAMIN A;

EID: 84905970880     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1400062111     Document Type: Article

References (78)

1. Bataller R, Brenner DA (2005) Liver fibrosis. J Clin Invest 115(2):209-218
2. Forbes SJ, Parola M (2011) Liver fibrogenic cells. Best Pract Res Clin Gastroenterol 25(2):207-217
3. Kisseleva T, et al. (2006) Bone marrow-derived fibrocytes participate in pathogenesis of liver fibrosis. J Hepatol 45(3):429-438
4. Kisseleva T, et al. (2011) Fibrocyte-like cells recruited to the spleen support innate and adaptive immune responses to acute injury or infection. JMolMed (Berl) 89(10):997-1013
5. Scholten D, et al. (2011) Migration of fibrocytes in fibrogenic liver injury. Am J Pathol 179(1):189-198
6. Kalluri R (2009) EMT: When epithelial cells decide to become mesenchymal-like cells. J Clin Invest 119(6):1417-1419
7. Choi SS, Diehl AM (2009) Epithelial-to-mesenchymal transitions in the liver. Hepatology 50(6):2007-2013
8. Taura K, et al. (2010) Hepatocytes do not undergo epithelial-mesenchymal transition in liver fibrosis in mice. Hepatology 51(3):1027-1036
9. Scholten D, et al. (2010) Genetic labeling does not detect epithelial-to-mesenchymal transition of cholangiocytes in liver fibrosis in mice. Gastroenterology 139(3):987-998
10. Chu AS, et al. (2011) Lineage tracing demonstrates no evidence of cholangiocyte epithelial-to-mesenchymal transition in murine models of hepatic fibrosis. Hepatology 53(5):1685-1695
11. Dranoff JA, Wells RG (2010) Portal fibroblasts: Underappreciated mediators of biliary fibrosis. Hepatology 51(4):1438-1444
12. Bhunchet E, Wake K (1992) Role of mesenchymal cell populations in porcine seruminduced rat liver fibrosis. Hepatology 16(6):1452-1473
13. Desmoulière A, et al. (1997) Extracellular matrix deposition, lysyl oxidase expression, and myofibroblastic differentiation during the initial stages of cholestatic fibrosis in the rat. Lab Invest 76(6):765-778
14. Uchio K, et al. (2002) Cellular retinol-binding protein-1 expression and modulation during in vivo and in vitro myofibroblastic differentiation of rat hepatic stellate cells and portal fibroblasts. Lab Invest 82(5):619-628
15. Wen JW, Olsen AL, Perepelyuk M, Wells RG (2012) Isolation of rat portal fibroblasts by in situ liver perfusion. J Vis Exp (64):3669
16. Kruglov EA, Jain D, Dranoff JA (2002) Isolation of primary rat liver fibroblasts. J Investig Med 50(3):179-184
17. Clouzeau-Girard H, et al. (2006) Effects of bile acids on biliary epithelial cell proliferation and portal fibroblast activation using rat liver slices. Lab Invest 86(3): 275-285
18. Knittel T, et al. (1999) Rat liver myofibroblasts and hepatic stellate cells: Different cell populations of the fibroblast lineage with fibrogenic potential. Gastroenterology 117(5):1205-1221
19. Goodpaster T, et al. (2008) An immunohistochemical method for identifying fibroblasts in formalin-fixed, paraffin-embedded tissue. J Histochem Cytochem 56(4): 347-358
20. Dranoff JA, et al. (2002) The ecto-nucleoside triphosphate diphosphohydrolase NTPDase2/CD39L1 is expressed in a novel functional compartment within the liver. Hepatology 36(5):1135-1144
21. Bosselut N, et al. (2010) Distinct proteomic features of two fibrogenic liver cell populations: Hepatic stellate cells and portal myofibroblasts. Proteomics 10(5):1017-1028
22. Yata Y, et al. (2003) DNase I-hypersensitive sites enhance alpha1(I) collagen gene expression in hepatic stellate cells. Hepatology 37(2):267-276
23. Brenner DA, Rippe RA, Veloz L (1989) Analysis of the collagen alpha 1(I) promoter. Nucleic Acids Res 17(15):6055-6064
24. Österreicher CH, et al. (2010) Fibroblast specific protein 1 identifies a subpopulation of liver inflammatory macrophages. Proc Natl Acad Sci USA 108(1):308-13
25. De Minicis S, et al. (2007) Gene expression profiles during hepatic stellate cell activation in culture and in vivo. Gastroenterology 132(5):1937-1946
26. Inokuchi S, et al. (2011) Toll-like receptor 4 mediates alcohol-induced steatohepatitis through bone marrow-derived and endogenous liver cells in mice. Alcohol Clin Exp Res 35(8):1509-1518
27. Lin SL, Kisseleva T, Brenner DA, Duffield JS (2008) Pericytes and perivascular fibroblasts are the primary source of collagen-producing cells in obstructive fibrosis of the kidney. Am J Pathol 173(6):1617-1627
28. Meng F, et al. (2012) Interleukin-17 signaling in inflammatory, Kupffer cells, and hepatic stellate cells exacerbates liver fibrosis in mice. Gastroenterology 143(3): 765-776, e761-763
29. Meurer SK, et al. (2013) Overexpression of endoglin modulates TGF-β1-signalling pathways in a novel immortalized mouse hepatic stellate cell line. PLoS ONE 8(2): e56116
30. Parsons CJ, et al. (2011) Mutation of the 5'-untranslated region stem-loop structure inhibits α1(I) collagen expression in vivo. J Biol Chem 286(10):8609-8619
31. Stefanovic B, Brenner DA (2003) 5' stem-loop of collagen alpha 1(I) mRNA inhibits translation in vitro but is required for triple helical collagen synthesis in vivo. J Biol Chem 278(2):927-933
32. Stefanovic B, et al. (1997) Posttranscriptional regulation of collagen alpha1(I) mRNA in hepatic stellate cells. Mol Cell Biol 17(9):5201-5209
33. Stefanovic B, Lindquist J, Brenner DA (2000) The 5' stem-loop regulates expression of collagen alpha1(I) mRNA in mouse fibroblasts cultured in a three-dimensional matrix. Nucleic Acids Res 28(2):641-647
34. Stefanovic B, Schnabl B, Brenner DA (2002) Inhibition of collagen alpha 1(I) expression by the 5' stem-loop as a molecular decoy. J Biol Chem 277(20):18229-18237
35. Stefanovic L, Brenner DA, Stefanovic B (2005) Direct hepatotoxic effect of KC chemokine in the liver without infiltration of neutrophils. Exp Biol Med (Maywood) 230(8):573-586
36. Taura K, et al. (2008) Hepatic stellate cells secrete angiopoietin 1 that induces angiogenesis in liver fibrosis. Gastroenterology 135(5):1729-1738
37. Magness ST, Bataller R, Yang L, Brenner DA (2004) A dual reporter gene transgenic mouse demonstrates heterogeneity in hepatic fibrogenic cell populations. Hepatology 40(5):1151-1159
38. Magness ST, Brenner DA (1999) Targeted disruption of the mouse ferrochelatase gene producing an exon 10 deletion. Biochim Biophys Acta 1453(1):161-174
39. Bataller R, et al. (2003) NADPH oxidase signal transduces angiotensin II in hepatic stellate cells and is critical in hepatic fibrosis. J Clin Invest 112(9):1383-1394
40. Kisseleva T, et al. (2012) Myofibroblasts revert to an inactive phenotype during regression of liver fibrosis. Proc Natl Acad Sci USA 109(24):9448-9453
41. Seki E, et al. (2007) TLR4 enhances TGF-beta signaling and hepatic fibrosis. Nat Med 13(11):1324-1332
42. Perepelyuk M, et al. (2013) Hepatic stellate cells and portal fibroblasts are the major cellular sources of collagens and lysyl oxidases in normal liver and early after injury. Am J Physiol Gastrointest Liver Physiol 304(6):G605-G614
43. Fort MM, et al. (2001) IL-25 induces IL-4, IL-5, and IL-13 and Th2-associated pathologies in vivo. Immunity 15(6):985-995
44. Gregory LG, et al. (2012) 25 drives remodelling in allergic airways disease induced by house dust mite. Thorax 68(1):82-90
45. Liu Y, et al. (2011) IL-13 induces connective tissue growth factor in rat hepatic stellate cells via TGF-β-independent Smad signaling. J Immunol 187(5):2814-2823
46. Pope SM, et al. (2005) Identification of a cooperative mechanism involving interleukin-13 and eotaxin-2 in experimental allergic lung inflammation. J Biol Chem 280(14):13952-13961
47. Jinnin M, et al. (2006) Upregulation of tenascin-C expression by IL-13 in human dermal fibroblasts via the phosphoinositide 3-kinase/Akt and the protein kinase C signaling pathways. J Invest Dermatol 126(3):551-560
48. Onitsuka I, Tanaka M, Miyajima A (2010) Characterization and functional analyses of hepatic mesothelial cells in mouse liver development. Gastroenterology 138(4): 1525-1535, e1521-1526
49. Bochmann L, et al. (2010) Revealing new mouse epicardial cell markers through transcriptomics. PLoS ONE 5(6):e11429
50. Asahina K (2012) Hepatic stellate cell progenitor cells. J Gastroenterol Hepatol 27 (Suppl 2):80-84
51. Asahina K, et al. (2009) Mesenchymal origin of hepatic stellate cells, submesothelial cells, and perivascular mesenchymal cells during mouse liver development. Hepatology 49(3):998-1011
52. Glaser SS, et al. (2007) Knockout of alpha-calcitonin gene-related peptide reduces cholangiocyte proliferation in bile duct ligated mice. Lab Invest 87(9):914-926
53. Chang K, Pastan I (1996) Molecular cloning of mesothelin, a differentiation antigen present on mesothelium, mesotheliomas, and ovarian cancers. Proc Natl Acad Sci USA 93(1):136-140
54. Grigoriu BD, Grigoriu C, Chahine B, Gey T, Scherpereel A (2009) Clinical utility of diagnostic markers for malignant pleural mesothelioma. Monaldi Arch Chest Dis 71(1): 31-38
55. Bera TK, Pastan I (2000) Mesothelin is not required for normal mouse development or reproduction. Mol Cell Biol 20(8):2902-2906
56. Lujambio A, et al. (2013) Non-cell-autonomous tumor suppression by p53. Cell 153(2): 449-460
57. Krizhanovsky V, et al. (2008) Senescence of activated stellate cells limits liver fibrosis. Cell 134(4):657-667
58. Henderson NC, et al. (2013) Targeting of αv integrin identifies a core molecular pathway that regulates fibrosis in several organs. Nat Med 19(12):1617-1624
59. Mederacke I, et al. (2013) Fate tracing reveals hepatic stellate cells as dominant contributors to liver fibrosis independent of its aetiology. Nat Commun 4:2823
60. Asahina K, Zhou B, Pu WT, Tsukamoto H (2011) Septum transversum-derived mesothelium gives rise to hepatic stellate cells and perivascular mesenchymal cells in developing mouse liver. Hepatology 53(3):983-995
61. Desmoulière A (2007) Hepatic stellate cells: The only cells involved in liver fibrogenesis? A dogma challenged. Gastroenterology 132(5):2059-2062
62. Tang L, Tanaka Y, Marumo F, Sato C (1994) Phenotypic change in portal fibroblasts in biliary fibrosis. Liver 14(2):76-82
63. Tuchweber B, Desmoulière A, Bochaton-Piallat ML, Rubbia-Brandt L, Gabbiani G (1996) Proliferation and phenotypic modulation of portal fibroblasts in the early stages of cholestatic fibrosis in the rat. Lab Invest 74(1):265-278
64. Syal G, Fausther M, Dranoff JA (2012) Advances in cholangiocyte immunobiology. Am J Physiol Gastrointest Liver Physiol 303(10):G1077-G1086
65. Fickert P, et al. (2009) Farnesoid X receptor critically determines the fibrotic response in mice but is expressed to a low extent in human hepatic stellate cells and periductal myofibroblasts. Am J Pathol 175(6):2392-2405
66. Fausther M, Dranoff JA (2011) New insights on the pathogenesis of biliary cirrhosis provided by studies in FXR knockout mice. J Hepatol 55(4):939-940
67. Guyot C, et al. (2010) Fibrogenic cell phenotype modifications during remodelling of normal and pathological human liver in cultured slices. Liver Int 30(10):1529-1540
68. Keitel V, et al. (2009) The membrane-bound bile acid receptor TGR5 is localized in the epithelium of human gallbladders. Hepatology 50(3):861-870
69. Fabris L, Strazzabosco M (2011) Epithelial-mesenchymal interactions in biliary diseases. Semin Liver Dis 31(1):11-32
70. Wynn TA (2003) IL-13 effector functions. Annu Rev Immunol 21:425-456
71. Liu Y, Munker S, Müllenbach R, Weng HL (2012) IL-13 signaling in liver fibrogenesis. Front Immunol 3:116
72. Roderfeld M, et al. (2012) Bone marrow transplantation improves hepatic fibrosis in Abcb4-/-mice via Th1 response and matrix metalloproteinase activity. Gut 61(6): 907-916
73. Enzan H, et al. (1997) Development of hepatic sinusoidal structure with special reference to the Ito cells. Microsc Res Tech 39(4):336-349
74. Zhou B, et al. (2008) Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 454(7200):109-113
75. Hassan R, Bera T, Pastan I (2004) Mesothelin: A new target for immunotherapy. Clin Cancer Res 10(12 Pt 1):3937-3942
76. Scholler N, et al. (1999) Soluble member(s) of the mesothelin/ megakaryocyte potentiating factor family are detectable in sera from patients with ovarian carcinoma. Proc Natl Acad Sci USA 96(20):11531-11536
77. Sapede C, et al. (2008) Aberrant splicing and protease involvement in mesothelin release from epithelioid mesothelioma cells. Cancer Sci 99(3):590-594
78. Woo K, et al. (2010) Adenosine triphosphate release and purinergic (P2) receptormediated secretion in small and large mouse cholangiocytes. Hepatology 52(5): 1819-1828.