Human liver myofibroblasts during development and diseases with a focus on portal (myo)fibroblasts

Frontiers in Physiology

Volumn 6, Issue MAY, 2015, Pages

  Lepreux, Sébastien ^b   Desmoulière, Alexis ^a  

^a UNIVERSITY OF LIMOGES   (France)

^b BORDEAUX UNIVERSITY HOSPITAL   (France)

Author keywords

Alpha smooth muscle actin; Fibrosis; Hepatic stellate cell; Liver development; Myofibroblast; Portal fibroblast; Tumoral stroma

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CALDESMON; SMOOTHELIN;

APOPTOSIS; BILE DUCT; CELL DIFFERENTIATION; CELL MATURATION; CHRONIC HEPATITIS; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; GRANULATION TISSUE; HUMAN; LIVER CELL; LIVER CIRRHOSIS; LIVER DEVELOPMENT; LIVER DISEASE; LIVER FIBROSIS; LIVER INJURY; LIVER REGENERATION; LIVER SINUSOID; MORPHOGENESIS; MYOFIBROBLAST; PARTIAL HEPATECTOMY; PORTAL VEIN; SCAR FORMATION; SHORT SURVEY; STELLATE CELL; STEM CELL; STROMA CELL; TISSUE REPAIR;

EID: 84930680902     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2015.00173     Document Type: Short Survey

References (79)

1. Andrade, Z.A., Guerret, S., and Fernandes, A.L. (1999). Myofibroblasts in schistosomal portal fibrosis of man. Mem. Inst. Oswaldo Cruz 94, 87-93.
2. Asahina, K., Zhou, B., Pu, W.T., and Tsukamoto, H. (2011). Septum transversum-derived mesothelium gives rise to hepatic stellate cells and perivascular mesenchymal cells in developing mouse liver. Hepatology 53, 983-995. doi: 10.1002/hep.24119.
3. Bachem, M.G., Riess, U., and Gressner, A.M. (1989). Liver fat storing cell proliferation i357 s stimulated by epidermal growth factor/transforming growth factor alpha and inhibited by transforming growth factor beta. Biochem. Biophys. Res. Commun. 162, 708-714.
4. Beaussier, M., Wendum, D., Schiffer, E., Dumont, S., Rey, C., Lienhart, A., et al. (2007). Prominent contribution of portal mesenchymal cells to liver fibrosis in ischemic and obstructive cholestatic injuries. Lab. Invest. 87, 292-303.
5. Bhunchet, E., and Wake, K. (1992). Role of mesenchymal cell populations in porcine serum364 induced rat liver fibrosis. Hepatology 16, 1452-1473.
6. Blanc, J.F., Bioulac-Sage, P., Balabaud, C., and Desmoulière, A. (2005). Investigation of liver fibrosis in clinical practice. Hepatol. Res. 32, 1-8.
7. Bosch, J. (2007). Vascular deterioration in cirrhosis: the big picture. J. Clin. Gastroenterol. 41, S247-S253.
8. Ceballos, K.M., Nielsen, G.P., Selig, M.K., and O'Connell, J.X. (2000). Is anti-h-caldesmon useful for distinguishing smooth muscle and myofibroblastic tumors? An immunohistochemical study. Am. J. Clin. Pathol. 114, 746-753.
9. Chen, Y., Choi, S.S., Michelotti, G.A., Chan, I.S., Swiderska-Syn, M., Kraca, G.F., et al. (2012a). Hedgehog controls hepatic stellate cell fate by regulating metabolism. Gastroenterology 143, 1319-1329. doi: 10.1053/j.gastro.2012.07.115.
10. Chen, Y., Zheng, S., Qi, D., Zheng, S., Guo, J., Zhang, S., et al. (2012b). Inhibition of Notch signaling by a γ-secretase inhibitor attenuates hepatic fibrosis in rats. PLoS One 7, e46512. doi: 10.1371/journal.pone.0046512.
11. Choi, S.S., and Diehl, A.M. (2009). Epithelial-to-mesenchymal transitions in the liver. Hepatology 50, 2007-2013.
12. Crawford, A.R., Lin, X.Z., and Crawford, J.M. (1998). The normal adult human liver biopsy: a quantitative reference standard. Hepatology 28, 323-331.
13. Costa, A.M., Tuchweber, B., Rubbia-Brandt, L., Peyrol, S., Chevallie, M., Adham, M., et al. (2001). Early activation of hepatic stellate cells and perisinusoidal extracellular matrix changes during ex vivo pig liver perfusion. J Submicrosc Cytol Pathol. 33, 231-240.
14. Darby, I.A., Vuillier-Devillers, K., Pinault, E., Sarrazy, V., Lepreux, S., Balabaud, C., et al. (2011). Cancer Microenviron. 4, 73-91. doi: 10.1007/s12307-010-0047-2.
15. Desmoulière, A. (2007). Hepatic stellate cells: the only cells involved in liver fibrogenesis? a dogma challenged. Gastroenterology 132, 2059-2062.
16. Desmoulière, A., Redard, M., Darby, I., and Gabbiani, G. (1995). Apoptosis mediates the decrease in cellularity during the transition between granulation tissue and scar. Am. J. Pathol. 146, 56-66.
17. Enzan, H., Himeno, H., Hiroi, M., Kiyoku, H., Saibara, T., and Onishi, S. (1997). Development of hepatic sinusoidal structure with special reference to the Ito cells. Microsc. Res. Tech. 39, 336-349.
18. Fausther, M., Lavoie, E.G., and Dranoff, J.A. (2013). Contribution of myofibroblasts of different origins to liver fibrosis. Curr. Pathobiol. Rep. 1, 225-230.
19. French, S.W., Miyamoto, K., Wong, K., Jui, L., and Briere, L. (1988). Role of the Ito cell in liver parenchymal fibrosis in rats fed alcohol and a high fat-low protein diet. Am. J. Pathol. 132, 73-85.
20. Frid, M.G., Shekhonin, B.V., Koteliansky, V.E., and Glukhova, M.A. (1992). Phenotypic changes of human smooth muscle cells during development: late expression of heavy caldesmon and calponin. Dev. Biol. 153, 185-193.
21. Fujimiya, T., Liu, J., Kojima, H., Shirafuji, S., Kimura, H., and Fujimiya, M. (2009). Pathological roles of bone marrow-derived stellate cells in a mouse model of alcohol405 induced fatty liver. Am. J. Physiol. Gastrointest. Liver Physiol. 297, G451-460. doi: 10.1152/ajpgi.00055.2009.
22. Gabbiani, G., Ryan, G.B., and Majno, G. (1971). Presence of modified fibroblasts i407 n granulation tissue and their possible role in wound contraction. Experientia 27, 549-550.
23. Geerts, A. (2001). History, heterogeneity, developmental biology, and functions of quiescent hepatic stellate cells. Semin. Liver Dis. 21, 311-335.
24. Geerts, A. (2004). On the origin of stellate cells: mesodermal, endodermal or neuro412 ectodermal? J. Hepatol. 40, 331-334.
25. Grappone, C., Pinzani, M., Parola, M., Pellegrini, G., Caligiuri, A., DeFranco, R., et al. (1999). Expression of platelet-derived growth factor in newly formed cholangiocytes during experimental biliary fibrosis in rats. J. Hepatol. 31, 100-109.
26. Gressner, A.M., and Bachem, M.G. (1995). Molecular mechanisms of liver fibrogenesis-a homage to the role of activated fat-storing cells. Digestion 56, 335-346.
27. Guyot, C., Combe, C., Balabaud, C., Bioulac-Sage, P., and Desmoulière, A. (2007). Fibrogenic cell fate during fibrotic tissue remodelling observed in rat and human cultured liver slices. J. Hepatol. 46, 142-150.
28. Guyot, C., Lepreux, S., Combe, C., Doudnikoff, E., Bioulac-Sage, P., Balabaud, C., et al. (2006). Hepatic fibrosis and cirrhosis: the (myo)fibroblastic cell subpopulations involved. Int. J. Biochem. Cell Biol. 38, 135-151.
29. Guyot, C., Lepreux, S., Combe, C., Sarrazy, V., Billet, F., Balabaud, C., Bioulac-Sage, P., and Desmoulière, A. (2010). Fibrogenic cell phenotype modifications during remodelling of normal and pathological human liver in cultured slices. Liver Int. 30, 1529-1540. doi: 10.1111/j.1478-3231.2010.02342.x.
30. Hautekeete, M.L., and Geerts, A. (1997). The hepatic stellate (Ito) cell: its role in human liver disease. Virchows Arch. 430, 195-207.
31. He, Y., Wu, G.D., Sadahiro, T., Noh, S.I., Wang, H., Talavera, D., et al. (2008). Interaction of CD44 and hyaluronic acid enhances biliary epithelial proliferation in cholestatic livers. Am. J. Physiol. Gastrointest. Liver Physiol. 295, G305-G312. doi: 10.1152/ajpgi.90229.2008.
32. Heindryckx, F., and Gerwins, P. (2015). Targeting the tumor stroma in hepatocellular carcinoma. World J. Hepatol. 7, 165-176. doi: 10.4254/wjh.v7.i2.165.
33. Hinz, B., Phan, S.H., Thannickal, V.J., Prunotto, M., Desmoulière, A., Varga, J. et al. (2012). Recent developments in myofibroblast biology: paradigms for connective tissue remodeling. Am. J. Pathol. 180, 1340-1355. doi: 10.1016/j.ajpath.2012.02.004.
34. Iredale, J.P., Benyon, R.C., Pickering, J., McCullen, M., Northrop, M., Pawley, S., et al. (1998). Mechanisms of spontaneous resolution of rat liver fibrosis. Hepatic stellate cell apoptosis and reduced hepatic expression of metalloproteinase inhibitors. J. Clin. Invest. 102, 538-549.
35. Jhandier, N.M., Kruglov, E.A., Lavoie, E.G., Sévigny, J., and Dranoff, J.A. (2005). Portal fibroblasts regulate the proliferation of bile duct epithelia via expression of NTPDase2. J. Biol. Chem. 280, 22986-22992.
36. Kalluri, R., and Weinberg, R.A. (2009). The basics of epithelial-mesenchymal transition. J. Clin. Invest.119, 1420-1428.
37. Kanta, J., Dooley, S., Delvoux, B., Breuer, S., D'Amico, T., and Gressner, A.M. (2002). Tropoelastin expression is up-regulated during activation of hepatic stellate cells and in the livers of CCl4-cirrhotic rats. Liver 22, 220-227.
38. Kinnman, N., and Housset, C. (2002). Peribiliary myofibroblasts in biliary type liver fibrosis. Front. Biosci. 7, d496-503.
39. Kinnman, N., Francoz, C., Barbu, V., Wendum, D., Rey, C., Hultcrantz, R., et al. (2003). The myofibroblastic conversion of peribiliary fibrogenic cells distinct from hepatic stellate cells is stimulated by platelet-derived growth factor during liver fibrogenesis. Lab. Invest. 83, 163-173.
40. Kisseleva, T., and Brenner, D.A. (2012). The phenotypic fate and functional role for bon457 e marrow-derived stem cells in liver fibrosis. J. Hepatol. 56, 965-72. doi: 10.1016/j.jhep.2011.09.021.
41. Kisseleva, T., Cong, M., Paik, Y., Scholten, D., Jiang, C., Benner, C., et al. (2012). Myofibroblasts revert to an inactive phenotype during regression of liver fibrosis. Proc. Natl. Acad. Sci. USA 109, 9448-9453. doi: 10.1073/pnas.1201840109.
42. Kordes, C., Sawitza, I., Götze, S., Herebian, D., and Häussinger, D. (2014). Hepatic stellate cells contribute to progenitor cells and liver regeneration. J. Clin. Invest. 124, 5503-5515. doi: 10.1172/JCI74119.
43. Lamireau, T., Le Bail, B., Boussarie, L., Fabre, M., Vergnes, P., Bernard, O., et al. (1999). Expression of collagens type I and IV, osteonectin and transforming growth factor beta-1 (TGFbeta1) in biliary atresia and paucity of intrahepatic bile ducts during infancy. J. Hepatol. 31, 248-255.
44. Lemoinne, S., Cadoret, A., El Mourabit, H., Thabut, D., and Housset, C. (2013). Origins and functions of liver myofibroblasts. Biochim. Biophys. Acta. 1832, 948-954. doi: 10.1016/j.bbadis.2013.02.019.
45. Lepreux, S., Bioulac-Sage, P., Gabbiani, G., Sapin, V., Housset, C., Rosenbaum, J., et al. (2004). Cellular retinol-binding protein-1 expression in normal and fibrotic/cirrhotic human liver: different patterns of expression in hepatic stellate cells and (myo)fibroblast subpopulations. J. Hepatol. 40, 774-780.
46. Lepreux, S., Dubuisson, L., Le Bail, B., Desmoulière, A., Balabaud, C., and Bioulac-Sage, P. (2001). Can hepatic stellate cells express alpha-smooth muscle actin in normal human liver? Liver 21, 293-294.
47. Lepreux, S., Guyot, C., Billet, F., Combe, C., Balabaud, C., Bioulac-Sage P, et al. (2013). Smoothelin, a new marker to determine the origin of liver fibrogenic cells. World J. Gastroenterol. 19, 9343-9350.
48. Libbrecht, L., Cassiman, D., Desmet, V., and Roskams, T. (2002). The correlation between portal myofibroblasts and development of intrahepatic bile ducts and arterial branches in human liver. Liver 22, 252-258.
49. Lorena, D., Darby, I.A., Reinhardt, D.P., Sapin, V., Rosenbaum, J., and Desmoulière, A. (2004). Fibrillin-1 expression in normal and fibrotic rat liver and in cultured hepatic fibroblastic cells: modulation by mechanical stress and role in cell adhesion. Lab. Invest. 84, 203-212.
50. Mak, K.M., and Lieber, C.S. (1988). Lipocytes and transitional cells in alcoholic liver disease: a morphometric study. Hepatology 8, 1027-1033.
51. Mederacke, I., Hsu, C.C., Troeger, J.S., Huebener, P., Mu, X., Dapito, D. H., et al. (2013). Fate tracing reveals hepatic stellate cells as dominant contributors to liver fibrosis independent of its aetiology. Nat. Commun. 4, 2823. doi:10.1038/ncomms3823.
52. Milani, S., Herbst, H., Shuppan, D., Stein, H., and Surrenti, C. (1991). Transforming growth factors beta 1 and beta 2 are differentially expressed in fibrotic liver disease. Am. J. Pathol. 139, 1221-1229.
53. Omenetti, A., Bass, L.M., Anders, R.A., Clemente, M.G., Francis, H., Guy, C.D., et al. (2011). Hedgehog activity, epithelial-mesenchymal transitions, and biliary dysmorphogenesis in biliary atresia. Hepatology 53, 1246-1258. doi: 10.1002/hep.24156.
54. Ozaki, S., Sato, Y., Yasoshima, M., Harada, K., and Nakanuma, Y. (2005). Diffuse expression of heparin sulfate proteoglycan and connective tissue growth factor in fibrous septa with many mast cells relate to unresolving hepatic fibrosis of congenital hepatic fibrosis. Liver Int. 25, 817-828.
55. Perepelyuk, M., Terajima, M., Wang, A.Y., Georges, P.C., Janmey, P.A., Yamauchi, 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, G605-G614. doi: 10.1152/ajpgi.00222.2012.
56. Ramadori, G. (1991). The stellate cell (Ito-cell, fat-storing cell, lipocyte, perisinusoidal cell) of the liver. New insights into pathophysiology of an intriguing cell. Virchows Arch. B Cell Pathol. Incl. Mol. Pathol. 61, 147-158.
57. Reeves, H.L., and Friedman, S.L. (2002). Activation of hepatic stellate cells-a key issue in liver fibrosis. Front. Biosci. 7, d808-826.
58. Rinn, J.L., Bondre, C., Gladstone, H.B., Brown, P.O., and Chang, H.Y. (2006). Anatomic demarcation by positional variation in fibroblast gene expression programs. PLoS Genet. 2, e119.
59. Rinn, J.L., Wang, J.K., Allen, N., Brugmann, S.A., Mikels, A.J., Liu, H., et al. (2008). A dermal HOX transcriptional program regulates site-specific epidermal fate. Genes Dev. 22, 303-307. doi: 10.1101/gad.1610508.
60. Rizvi, S., Borad, M.J., Patel, T., and Gores, G.J. (2014). Cholangiocarcinoma: molecular pathways and therapeutic opportunities. Semin. Liver Dis. 34, 456-464. doi: 10.1055/s-0034-1394144.
61. Roskams, T., and Desmet, V. (2008). Embryology of extra-and intrahepatic bile ducts, the ductal plate. Anat. Rec. (Hoboken) 291, 628-635. doi: 10.1002/ar.20710.
62. Sakaida, I. (2008). Autologous bone marrow cell infusion therapy for liver cirrhosis. J. Gastroenterol. Hepatol. 23, 1349-1353.
63. Schäfer, M., and Werner, S. (2008). Cancer as an overhealing wound: an old hypothesis revisited. Nat. Rev. Mol. Cell Biol. 9, 628-638. doi: 10.1038/nrm2455.
64. Schuppan, D., Ruehl, M., Somasundaram, R., and Hahn, E.G. (2001). Matrix as a modulator of hepatic fibrogenesis. Semin. Liver Dis. 21, 351-372.
65. Sedlaczek, N., Jia, J.D., Bauer, M., Herbst, H., Ruehl, M., Hahn, E.G., et al. (2001). Proliferating bile duct epithelial cells are a major source of connective tissue growth factor in rat biliary fibrosis. Am. J. Pathol. 158, 1239-1244.
66. Sohara, N., Znoyko, I., Levy, M.T., Trojanowska, M., and Reuben, A. (2002). Reversal of activation of human myofibroblast-like cells by culture on a basement membrane-like substrate. J. Hepatol. 37, 214-221.
67. Swiderska-Syn, M., Syn, W.K., Xie, G., Krüger, L., Machado, M.V., Karaca, G., et al. (2014). Myofibroblastic cells function as progenitors to regenerate murine livers after partial hepatectomy. Gut 63, 1333-1344. doi: 10.1136/gutjnl-2013-305962.
68. Tang, L., Tanaka, Y., Marumo, F., and Sato, C. (1994). Phenotypic change in portal fibroblasts in biliary fibrosis. Liver 14, 76-82.
69. Tanimizu, N., Kikkawa, Y., Mitaka, T., and Miyajima, A. (2012). α1-and α5-containing laminins regulate the development of bile ducts via β1 integrin signals. J. Biol. Chem. 287, 28586-28597. doi: 10.1074/jbc. M112.350488.
70. Terada, T., and Nakanuma, Y. (1994). Expression of tenascin, type IV collagen and laminin during human intrahepatic bile duct development and in intrahepatic cholangiocarcinoma. Histopathology 25, 143-150.
71. Tschumperlin, D.J. (2013). Fibroblasts and the ground they walk on. Physiology (Bethesda) 28, 380-390. doi: 10.1152/physiol.00024.2013.
72. Tuchweber, B., Desmoulière, A., Bochaton-Piallat, M.L., Rubbia-Brandt, L., and Gabbiani, G. (1996). Proliferation and phenotypic modulation of portal fibroblasts in the early stages of cholestatic fibrosis in rat. Lab. Invest. 74, 265-278.
73. van der Loop, F.T., Gabbiani, G., Kohnen, G., Ramaekers, F.C, and van Eys, G.J. (1997). Differentiation of smooth muscle cells in human blood vessels as defined by smoothelin, a novel marker for the contractile phenotype. Arterioscler. Thromb. Vasc. Biol. 17, 665-671. doi: 10.1161/01.ATV.17.4.665.
74. Villeneuve, J., Pelluard-Nehme, F., Combe, C., Carles, D., Chaponnier, C., Ripoche, J., et al. (2009). Immunohistochemical study of the phenotypic change of the mesenchymal cells during portal tract maturation in normal and fibrous (ductal plate malformation) fetal liver. Comp. Hepatol. 8, 5. doi: 10.1186/1476-5926-8-5.
75. Wake, K. (2006). Hepatic stellate cells: three-dimensional structure, localization, heterogeneity and development. Proc. Jpn. Acad., Ser. B 82, 155-164.
76. Wells, R.G. (2014). The portal fibroblast: not just a poor man's stellate cell. Gastroenterology 147, 41-47. doi: 10.1053/j.gastro.2014.05.001.
77. Win, K.M., Charlotte, F., Mallat, A., Cherqui, D., Martin, N., Mavier, P., et al. (1993). Mitogenic effect of transforming growth factor-beta 1 on human Ito cells in culture: evidence for mediation by endogenous platelet-derived growth factor. Hepatology 18, 137-145.
78. Xie, G., and Diehl, A.M. (2013). Evidence for and against epithelial-to-mesenchymal transition in the liver. Am. J. Physiol. Gastrointest. Liver Physiol. 305, G881-G890. doi: 10.1152/ajpgi.00289.2013.
79. Xie, G., Karaca, G., Swiderska-Syn, M., Michelotti, G.A., Krüger, L., Chen, Y., et al. (2013). Cross-talk between Notch and Hedgehog regulates hepatic stellate cell fate. Hepatology 58, 1801-1831. doi: 10.1002/hep.26511.