Cytoglobin is expressed in hepatic stellate cells, but not in myofibroblasts, in normal and fibrotic human liver

Laboratory Investigation

Volumn 94, Issue 2, 2014, Pages 192-207

  Motoyama, Hiroyuki ^a   Komiya, Tohru ^b   Thuy, Le Thi Thanh ^a   Tamori, Akihiro ^a   Enomoto, Masaru ^a   Morikawa, Hiroyasu ^a   Iwai, Shuji ^a   Uchida Kobayashi, Sawako ^a   Fujii, Hideki ^a   Hagihara, Atsushi ^a   Kawamura, Etsushi ^a   Murakami, Yoshiki ^a   Yoshizato, Katsutoshi ^a,c   Kawada, Norifumi ^a  

^a OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b Osaka Prefecture University   (Japan)

^c PhoenixBio USA Corporation   (Japan)

Author keywords

cellular retinol binding protein 1; chronic hepatitis; cytoglobin; fibulin 2; Thy 1; smooth muscle actin

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; ANTIBODY; CELLULAR RETINOL BINDING PROTEIN 1; CYTOGLOBIN; DYE; FIBULIN; FIBULIN 2; SIRIUS RED; THY 1 ANTIGEN; UNCLASSIFIED DRUG;

ADULT; AGED; ANIMAL CELL; ARTICLE; CELL CULTURE; CELL DAMAGE; CELL FUNCTION; CLINICAL ARTICLE; CONTROLLED STUDY; HEPATITIS C; HEPATITIS C VIRUS; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LIVER; LIVER BIOPSY; LIVER FIBROSIS; MIDDLE AGED; MYOFIBROBLAST; NONALCOHOLIC FATTY LIVER; NONHUMAN; PORTAL VEIN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STAINING; STELLATE CELL; TISSUE SECTION; VIRUS STRAIN;

ACTINS; ANIMALS; ANTIBODIES; ANTIGENS, THY-1; AZO COMPOUNDS; BIOLOGICAL MARKERS; CALCIUM-BINDING PROTEINS; CELLS, CULTURED; EXTRACELLULAR MATRIX PROTEINS; GLOBINS; HEPATIC STELLATE CELLS; HEPATITIS C; HUMANS; IMMUNOHISTOCHEMISTRY; LIVER CIRRHOSIS; MICE; MYOFIBROBLASTS;

EID: 84893234732     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2013.135     Document Type: Article

References (43)

1. Kawada N, Kristensen DB, Asahina K, et al. Characterization of a stellate cell activation-associated protein (STAP) with peroxidase activity found in rat hepatic stellate cells. J Biol Chem 2001;276:25318-25323.
2. Trent 3rd JT, Hargrove MS. A ubiquitously expressed human hexacoordinate hemoglobin. J Biol Chem 2002;277:19538-19545.
3. Burmester T, Ebner B, Weich B, et al. Cytoglobin: a novel globin type ubiquitously expressed in vertebrate tissues. Mol Biol Evol 2002;19: 416-421.
4. Pesce A, Bolognesi M, Bocedi A, et al. Neuroglobin and cytoglobin. Fresh blood for the vertebrate globin family. EMBO Rep 2002;3: 1146-1151.
5. Sawai H, Kawada N, Yoshizato K, et al. Characterization of the heme environmental structure of cytoglobin, a fourth globin in humans. Biochemistry 2003;42:5133-5142.
6. Schmidt M, Gerlach F, Avivi A, et al. Cytoglobin is a respiratory protein in connective tissue and neurons, which is up-regulated by hypoxia. J Biol Chem 2004;279:8063-8069.
7. Geuens E, Brouns I, Flamez D, et al. A globin in the nucleus! J Biol Chem 2003;278:30417-30420.
8. Friedman SL. Hepatic stellate cells: protean, multifunctional, and enigmatic cells of the liver. Physiol Rev. 2008;88:125-172.
9. Scholten D, Osterreicher CH, Scholten A, et al. Genetic labeling does not detect epithelial-to-mesenchymal transition of cholangiocytes in liver fibrosis in mice. Gastroenterology 2010;139:987-998.
10. Yokoi Y, Namihisa T, Kuroda H, et al. Immunocytochemical detection of desmin in fat-storing cells (Ito cells). Hepatology 1984;4:709-714.
11. Uchio K, Tuchweber B, Manabe N, et al. 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 2002;82:619-628.
12. Dudas J, Mansuroglu T, Batusic D, et al. Thy-1 is an in vivo and in vitro marker of liver myofibroblasts. Cell Tissue Res 2007;329:503-514.
13. Dezso K, Jelnes P, László V, et al. Thy-1 is expressed in hepatic myofibroblasts and not oval cells in stem cell-mediated liver regeneration. Am J Pathol 2007;171:1529-1537.
14. Dudas J, Mansuroglu T, Batusic D, et al. Thy-1 is expressed in myofibroblasts but not found in hepatic stellate cells following liver injury. Histochem Cell Biol 2009;131:115-127.
15. Knittel T, Kobold D, Saile B, et al. Rat liver myofibroblasts and hepatic stellate cells: different cell populations of the fibroblast lineage with fibrogenic potential. Gastroenterology 1999;117:1205-1221.
16. Uyama N, Iimuro Y, Kawada N, et al. Fascin, a novel marker of human hepatic stellate cells, may regulate their proliferation, migration, and collagen gene expression through the FAK-PI3K-Akt pathway. Lab Invest 2012;92:57-71.
17. Piscaglia F, Dudás J, Knittel T, et al. Expression of ECM proteins fibulin-1 and -2 in acute and chronic liver disease and in cultured rat liver cells. Cell Tissue Res 2009;337:449-462.
18. Janiec DJ, Jacobson ER, Freeth A, et al. Histologic variation of grade and stage of non-alcoholic fatty liver disease in liver biopsies. Obes Surg 2005;15:497-501.
19. Ichida F, Tsuji T, Omata M, et al. New lnuyama classification; new criteria for histological assessment of chronic hepatitis. Int Hepatol Com 1996;6:112-119.
20. Mori M, Fujii H, Ogawa T, et al. Close correlation of liver stiffness with collagen deposition and presence of myofibroblasts in non-alcoholic fatty liver disease. Hepatol Res 2011;41:897-903.
21. Ogawa T, Tateno C, Asahina K, et al. Identification of vitamin A-free cells in a stellate cell-enriched fraction of normal rat liver as myofibroblasts. Histochem Cell Biol 2007;127:161-174.
22. Xu L, Hui AY, Albanis E, et al. Human hepatic stellate cell lines, LX-1 and LX-2: new tools for analysis of hepatic fibrosis. Gut 2005;54:142-151.
23. Kristensen DB, Kawada N, Imamura K, et al. Proteome analysis of rat hepatic stellate cells. Hepatology 2000;32:268-277.
24. Mu YP, Ogawa T, Kawada N. Reversibility of fibrosis, inflammation, and endoplasmic reticulum stress in the liver of rats fed a methioninecholine- deficient diet. Lab Invest 2010;90:245-256.
25. Nakatani K, Okuyama H, Shimahara Y, et al. Cytoglobin/STAP, its unique localization in splanchnic fibroblast-like cells and function in organ fibrogenesis. Lab Invest 2004;84:91-101.
26. Sugimoto H, Makino M, Sawai H, et al. Structural basis of human cytoglobin for ligand binding. J Mol Biol 2004;339:873-885.
27. Mathew J, Hines JE, Toole K, et al. Quantitative analysis of macrophages and perisinusoidal cells in primary biliary cirrhosis. Histopathology 1994;25:65-70.
28. Mouta Carreira C, Nasser SM, di Tomaso E, et al. LYVE-1 is not restricted to the lymph vessels: expression in normal liver blood sinusoids and down-regulation in human liver cancer and cirrhosis. Cancer Res 2001;61:8079-8084.
29. Bosselut N, Housset C, Marcelo P, et al. Distinct proteomic features of two fibrogenic liver cell populations: hepatic stellate cells and portal myofibroblasts. Proteomics 2010;10:1017-1028.
30. Gabbiani G, Majno G. Dupuytren's contracture: fibroblast contraction? An ultrastructural study. Am J Pathol 1972;66:131-146.
31. Darby I, Skalli O, Gabbiani G. Alpha-smooth muscle actin is transiently expressed by myofibroblasts during experimental wound healing. Lab Invest 1990;63:21-29.
32. Gabbiani G. The myofibroblast in wound healing and fibrocontractive diseases. J Pathol 2003;200:500-503.
33. Desmouliere A, Tuchweber B, Gabbiani G. Role of the myofibroblast differentiation during liver fibrosis. J Hepatol 1995;22(2 Suppl):61-64.
34. Niki T, Rombouts K, De Bleser P, et al. A histone deacetylase inhibitor, trichostatin A, suppresses myofibroblastic differentiation of rat hepatic stellate cells in primary culture. Hepatology 1999;29:858-867.
35. Wake K. Perisinusoidal stellate cells (fat-storing cells, interstitial cells, lipocytes), their related structure in and around the liver sinusoids, and vitamin A-storing cells in extrahepatic organs. Int Rev Cytol 1980;66:303-353.
36. Rege TA, Hagood JS. Thy-1 as a regulator of cell-cell and cell-matrix interactions in axon regeneration, apoptosis, adhesion, migration, cancer, and fibrosis. FASEB J 2006;20:1045-1054.
37. Kawai S, Enzan H, Hayashi Y, et al. Vinculin: a novel marker for quiescent and activated hepatic stellate cells in human and rat livers. Virchows Arch 2003;443:78-86.
38. Uyama N, Zhao L, Van Rossen E, et al. Hepatic stellate cells express synemin, a protein bridging intermediate filaments to focal adhesions. Gut 2006;55:1276-1289.
39. Wake K, Sato T. Intralobular heterogeneity of perisinusoidal stellate cells in porcine liver. Cell Tissue Res 1993;273:227-237.
40. Nakatani K, Seki S, Kawada N, et al. Expression of neural cell adhesion molecule (N-CAM) in perisinusoidal stellate cells of the human liver. Cell Tissue Res 1996;283:159-165.
41. Cassiman D, Libbrecht L, Desmet V, et al. Hepatic stellate cell/myofibroblast subpopulations in fibrotic human and rat livers. J Hepatol 2002;36:200-209.
42. Cassiman D, Denef C, Desmet VJ, et al. Human and rat hepatic stellate cells express neurotrophins and neurotrophin receptors. Hepatology 2001;33:148-158.
43. 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 2013;110:2324-2329.