Role of TGF-β signaling in differentiation of mesothelial cells to vitamin a-poor hepatic stellate cells in liver fibrosis

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 310, Issue 4, 2016, Pages G262-G272

  Li, Yuchang ^a   Lua, Ingrid ^a   French, Samuel W ^b   Asahina, Kinji ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b HARBOR UCLA MEDICAL CENTER   (United States)

Author keywords

Capsular fibrosis; Fibrosis regression; Glisson s capsule; Myofibroblasts; Vitamin A

Indexed keywords

ACTA2 PROTEIN; COLLA1 PROTEIN; CONNECTIVE TISSUE GROWTH FACTOR; CYSTEINE RICH PROTEIN 61; PROTEIN; RETINOL; TIMP1 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; UNCLASSIFIED DRUG; PROTEIN SERINE THREONINE KINASE; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR-BETA TYPE II RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE COURSE; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; GENOTYPE; IMMUNOFLUORESCENCE; LIVER FIBROSIS; MESOTHELIUM; MESOTHELIUM CELL; MOUSE; MYOFIBROBLAST; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; STELLATE CELL; ANIMAL; BILE DUCT; CELL CULTURE; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM; FIBROBLAST; GENETICS; HEPATIC STELLATE CELL; INTOXICATION; KNOCKOUT MOUSE; LIGATION; LIVER; LIVER CIRRHOSIS; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; RETINOL DEFICIENCY;

ANIMALS; BILE DUCTS; CARBON TETRACHLORIDE POISONING; CELL DIFFERENTIATION; CELLS, CULTURED; EPITHELIAL-MESENCHYMAL TRANSITION; EPITHELIUM; FIBROBLASTS; HEPATIC STELLATE CELLS; LIGATION; LIVER; LIVER CIRRHOSIS; MICE; MICE, KNOCKOUT; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA; VITAMIN A DEFICIENCY;

EID: 84958536351     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00257.2015     Document Type: Article

References (35)

1. Abreu JG, Ketpura NI, Reversade B, De Robertis EM. Connectivetissue growth factor (CTGF) modulates cell signalling by BMP and TGF-β. Nat Cell Biol 4: 599–604, 2002.
2. Asahina K, Tsai SY, Li P, Ishii M, Maxson RE Jr, Sucov HM, Tsukamoto H. Mesenchymal origin of hepatic stellate cells, submesothelial cells, and perivascular mesenchymal cells during mouse liver development. Hepatology 49: 998–1011, 2009.
3. Asahina K, Zhou B, Pu WT, Tsukamoto H. Septum transversumderived mesothelium gives rise to hepatic stellate cells and perivascular mesenchymal cells in developing mouse liver. Hepatology 53: 983–995, 2011.
4. Borkham-Kamphorst E, Schaffrath C, Van de Leur E, Haas U, Tihaa L, Meurer SK, Nevzorova YA, Liedtke C, Weiskirchen R. The antifibrotic effects of CCN1/CYR61 in primary portal myofibroblasts are mediated through induction of reactive oxygen species resulting in cellular senescence, apoptosis and attenuated TGF-β signaling. Biochim Biophys Acta 1843: 902–914, 2014.
5. Chapman GB, Eagles DA. Ultrastructural features of Glisson’s capsule and the overlying mesothelium in rat, monkey and pike liver. Tissue Cell 39: 343–351, 2007.
6. Chen L, Charrier AL, Leask A, French SW, Brigstock DR. Ethanolstimulated differentiated functions of human or mouse hepatic stellate cells are mediated by connective tissue growth factor. J Hepatol 55: 399–406, 2011.
7. Dixit R, Ai X, Fine A. Derivation of lung mesenchymal lineages from the fetal mesothelium requires hedgehog signaling for mesothelial cell entry. Development 140: 4398–4406, 2013.
8. Ellis EL, Mann DA. Clinical evidence for the regression of liver fibrosis. J Hepatol 56: 1171–1180, 2012.
9. Friedman SL. Evolving challenges in hepatic fibrosis. Nat Rev Gastroenterol Hepatol 7: 425–436, 2010.
10. Hernandez-Gea V, Friedman SL. Pathogenesis of liver fibrosis. Annu Rev Pathol 6: 425–456, 2011.
11. Kisseleva T, Cong M, Paik Y, Scholten D, Jiang C, Benner C, Iwaisako K, Moore-Morris T, Scott B, Tsukamoto H, Evans SM, Dillmann W, Glass CK, Brenner DA. Myofibroblasts revert to an inactive phenotype during regression of liver fibrosis. Proc Natl Acad Sci USA 109: 9448–9453, 2012.
12. Krizhanovsky V, Yon M, Dickins RA, Hearn S, Simon J, Miething C, Yee H, Zender L, Lowe SW. Senescence of activated stellate cells limits liver fibrosis. Cell 134: 657–667, 2008.
13. Lamouille S, Xu J, Derynck R. Molecular mechanisms of epithelialmesenchymal transition. Nat Rev Mol Cell Biol 15: 178–196, 2014.
14. Leveen P, Larsson J, Ehinger M, Cilio CM, Sundler M, Sjostrand LJ, Holmdahl R, Karlsson S. Induced disruption of the transforming growth factor β type II receptor gene in mice causes a lethal inflammatory disorder that is transplantable. Blood 100: 560–568, 2002.
15. Li Y, Wang J, Asahina K. Mesothelial cells give rise to hepatic stellate cells and myofibroblasts via mesothelial-mesenchymal transition in liver injury. Proc Natl Acad Sci USA 110: 2324–2329, 2013.
16. Lua I, James D, Wang J, Wang KS, Asahina K. Mesodermal mesenchymal cells give rise to myofibroblasts, but not epithelial cells, in mouse liver injury. Hepatology 60: 311–322, 2014.
17. Lua I, Li Y, Pappoe LS, Asahina K. Myofibroblastic conversion and regeneration of mesothelial cells in peritoneal and liver fibrosis. Am J Pathol 185: 3258–3273, 2015.
18. Mutsaers SE. The mesothelial cell. Int J Biochem Cell Biol 36: 9–16, 2004.
19. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L. A global double-fluorescent Cre reporter mouse. Genesis 45: 593–605, 2007.
20. Ogawa T, Tateno C, Asahina K, Fujii H, Kawada N, Obara M, Yoshizato K. Identification of vitamin A-free cells in a stellate cellenriched fraction of normal rat liver as myofibroblasts. Histochem Cell Biol 127: 161–174, 2007.
21. Onitsuka I, Tanaka M, Miyajima A. Characterization and functional analyses of hepatic mesothelial cells in mouse liver development. Gastroenterology 138: 1525–1535, 2010.
22. Pellicoro A, Ramachandran P, Iredale JP. Reversibility of liver fibrosis. Fibrogenesis Tissue Repair 5: S26, 2012.
23. Que J, Wilm B, Hasegawa H, Wang F, Bader D, Hogan BL. Mesothelium contributes to vascular smooth muscle and mesenchyme during lung development. Proc Natl Acad Sci USA 105: 16626–16630, 2008.
24. Radaeva S, Sun R, Jaruga B, Nguyen VT, Tian Z, Gao B. Natural killer cells ameliorate liver fibrosis by killing activated stellate cells in NKG2Ddependent and tumor necrosis factor-related apoptosis-inducing liganddependent manners. Gastroenterology 130: 435–452, 2006.
25. Ramm GA, Britton RS, O’Neill R, Blaner WS, Bacon BR. Vitamin A-poor lipocytes: a novel desmin-negative lipocyte subpopulation, which can be activated to myofibroblasts. Am J Physiol Gastrointest Liver Physiol 269: G532–G541, 1995.
26. Sakai N, Chun J, Duffield JS, Wada T, Luster AD, Tager AM. LPA1-induced cytoskeleton reorganization drives fibrosis through CTGFdependent fibroblast proliferation. FASEB J 27: 1830–1846, 2013.
27. Schuppan D, Kim YO. Evolving therapies for liver fibrosis. J Clin Invest 123: 1887–1901, 2013.
28. Testerink N, Ajat M, Houweling M, Brouwers JF, Pully VV, van Manen HJ, Otto C, Helms JB, Vaandrager AB. Replacement of retinyl esters by polyunsaturated triacylglycerol species in lipid droplets of hepatic stellate cells during activation. PLoS One 7: e34945, 2012.
29. Troeger JS, Mederacke I, Gwak GY, Dapito DH, Mu X, Hsu CC, Pradere JP, Friedman RA, Schwabe RF. Deactivation of hepatic stellate cells during liver fibrosis resolution in mice. Gastroenterology 143: 1073–1083, 2012.
30. Winters NI, Thomason RT, Bader DM. Identification of a novel developmental mechanism in the generation of mesothelia. Development 139: 2926–2934, 2012.
31. Yang MD, Chiang YM, Higashiyama R, Asahina K, Mann DA, Mann J, Wang CC, Tsukamoto H. Rosmarinic acid and baicalin epigenetically derepress peroxisomal proliferator-activated receptor γ in hepatic stellate cells for their antifibrotic effect. Hepatology 55: 1271–1281, 2012.
32. Yata Y, Gotwals P, Koteliansky V, Rockey DC. Dose-dependent inhibition of hepatic fibrosis in mice by a TGF-β soluble receptor: implications for antifibrotic therapy. Hepatology 35: 1022–1030, 2002.
33. Yata Y, Scanga A, Gillan A, Yang L, Reif S, Breindl M, Brenner DA, Rippe RA. DNase I-hypersensitive sites enhance β1(I) collagen gene expression in hepatic stellate cells. Hepatology 37: 267–276, 2003.
34. Yin C, Evason KJ, Asahina K, Stainier DY. Hepatic stellate cells in liver development, regeneration, and cancer. J Clin Invest 123: 1902–1910, 2013.
35. Zhou B, Ma Q, Rajagopal S, Wu SM, Domian I, Rivera-Feliciano J, Jiang D, von Gise A, Ikeda S, Chien KR, Pu WT. Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 454: 109–113, 2008.