Mouse white adipose tissue-derived mesenchymal stem cells gain pericentral and periportal hepatocyte features after differentiation in vitro, which are preserved in vivo after hepatic transplantation

Acta Physiologica

Volumn 215, Issue 2, 2015, Pages 89-104

  Winkler, S ^a   Hempel, M ^a   Bruckner S ^a   Mallek, F ^b   Weise, A ^b   Liehr, T ^b   Tautenhahn, H M ^a,c   Bartels, M ^a   Christ, B ^a,c  

^a UNIVERSITY HOSPITAL LEIPZIG   (Germany)

^b JENA UNIVERSITY HOSPITAL   (Germany)

^c UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

Hepatocyte; Liver disease; Mesenchymal stem cells; Metabolic zonation; Regeneration; Transplantation

Indexed keywords

ALBUMIN; ALKALINE PHOSPHATASE; ALPHA 1 ANTITRYPSIN; ALPHA SMOOTH MUSCLE ACTIN; BETA1 INTEGRIN; CARBAMATE KINASE; CARBAMOYL PHOSPHATE SYNTHASE; CARBAMOYLPHOSPHATE SYNTHASE 1; CD14 ANTIGEN; CD34 ANTIGEN; CD45 ANTIGEN; CONNEXIN 43; CYCLOPHILIN A; CYTOCHROME P450 3A11; CYTOCHROME P450 3A4; CYTOKERATIN 18; CYTOKERATIN 19; CYTOKERATIN 7; DESMIN; DIPEPTIDYL PEPTIDASE IV; ENDOGLIN; ETHOXYRESORUFIN DEETHYLASE; GLUTAMATE AMMONIA LIGASE; HEPATOCYTE NUCLEAR FACTOR 4; HEPATOCYTE NUCLEAR FACTOR 4ALPHA; HERMES ANTIGEN; PENTOXYRESORUFIN DEALKYLASE; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); THY 1 ANTIGEN; UNCLASSIFIED DRUG; BIOLOGICAL MARKER;

ADIPOCYTE; ADULT; ALBUMIN BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARTILAGE CELL; CELL COMMUNICATION; CELL COUNT; CELL DIFFERENTIATION; CELL ISOLATION; CELL LINEAGE; CELL SHAPE; CELL STRUCTURE; CHROMOSOME ANALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HEPATOCYTE HEPATOCYTE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL; LIVER FUNCTION; LIVER TRANSPLANTATION; MALE; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; OSTEOCYTE; PERIPORTAL HEPATOCYTE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION; UREA CYCLE; WHITE ADIPOSE TISSUE; WHITE ADIPOSE TISSUE DERIVED MESENCHYMAL STEM CELL; ADIPOSE TISSUE; ANIMAL; BONE MARROW CELL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; LIVER; MESENCHYMAL STROMA CELL; METABOLISM; PHYSIOLOGY; SURGERY; WHITE ADIPOCYTE;

ADIPOCYTES, WHITE; ADIPOSE TISSUE; ANIMALS; BIOMARKERS; BONE MARROW CELLS; CELL DIFFERENTIATION; CELLS, CULTURED; HEPATOCYTES; LIVER; LIVER TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICE, INBRED C57BL;

EID: 84941745667     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/apha.12560     Document Type: Article

References (51)

1. Abad, M., Mosteiro, L., Pantoja, C., Canamero, M., Rayon, T., Ors, I., Grana, O., Megias, D., Dominguez, O., Martinez, D., Manzanares, M., Ortega, S. & Serrano, M. 2013. Reprogramming in vivo produces teratomas and iPS cells with totipotency features. Nature, 502, 340-345.
2. Aurich, I., Mueller, L.P., Aurich, H., Luetzkendorf, J., Tisljar, K., Dollinger, M.M., Schormann, W., Walldorf, J., Hengstler, J.G., Fleig, W.E. & Christ, B. 2007. Functional integration of hepatocytes derived from human mesenchymal stem cells into mouse livers. Gut 56, 405-415.
3. Aurich, H., Sgodda, M., Kaltwasser, P., Vetter, M., Weise, A., Liehr, T., Brulport, M., Hengstler, J.G., Dollinger, M.M., Fleig, W.E. & Christ, B. 2009. Hepatocyte differentiation of mesenchymal stem cells from human adipose tissue in vitro promotes hepatic integration in vivo. Gut 58, 570-581.
4. Banas, A. 2012. Purification of adipose tissue mesenchymal stem cells and differentiation toward hepatic-like cells. Methods Mol Biol 826, 61-72.
5. Banas, A., Teratani, T., Yamamoto, Y., Tokuhara, M., Takeshita, F., Quinn, G., Okochi, H. & Ochiya, T. 2007. Adipose tissue-derived mesenchymal stem cells as a source of human hepatocytes. Hepatology 46, 219-228.
6. Banas, A., Teratani, T., Yamamoto, Y., Tokuhara, M., Takeshita, F., Osaki, M., Kato, T., Okochi, H. & Ochiya, T. 2009. Rapid hepatic fate specification of adipose-derived stem cells and their therapeutic potential for liver failure. J Gastroenterol Hepatol 24, 70-77.
7. Bosch, P., Pratt, S.L. & Stice, S.L. 2006. Isolation, characterization, gene modification, and nuclear reprogramming of porcine mesenchymal stem cells. Biol Reprod 74, 46-57.
8. Bruckner, S., Tautenhahn, H.M., Winkler, S., Stock, P., Dollinger, M. & Christ, B. 2014. A fat option for the pig: hepatocytic differentiated mesenchymal stem cells for translational research. Exp Cell Res 321, 267-275.
9. Bulic-Jakus, F., Ulamec, M., Vlahovic, M., Sincic, N., Katusic, A., Juric-Lekc, G., Serman, L., Kruslin, B. & Belicza, M. 2006. Of mice and men: teratomas and teratocarcinomas. Coll Antropol 30, 921-924.
10. Burke, Z.D. & Tosh, D. 2006. The Wnt/beta-catenin pathway: master regulator of liver zonation? BioEssays 28, 1072-1077.
11. Butler, S.L., Dong, H., Cardona, D., Jia, M., Zheng, R., Zhu, H., Crawford, J.M. & Liu, C. 2008. The antigen for Hep Par 1 antibody is the urea cycle enzyme carbamoyl phosphate synthetase 1. Lab Invest 88, 78-88.
12. Castorina, S., Luca, T., Torrisi, A., Privitera, G. & Panebianco, M. 2008. Isolation of epithelial cells with hepatobiliary phenotype. Ital J Anat Embryol 113, 199-207.
13. Christ, B. & Pelz, S. 2013. Implication of hepatic stem cells in functional liver repopulation. Cytometry A 83, 90-102.
14. Dhawan, A., Strom, S.C., Sokal, E. & Fox, I.J. 2010. Human hepatocyte transplantation. Methods Mol Biol 640, 525-534.
15. Dominici, M., le Blanc, K., Mueller, I., Slaper-Cortenbach, I., Marini, F., Krause, D., Deans, R., Keating, A., Prockop, D. & Horwitz, E. 2006. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8, 315-317.
16. Farini, A., Sitzia, C., Erratico, S., Meregalli, M. & Torrente, Y. 2014. Clinical applications of mesenchymal stem cells in chronic diseases. Stem Cells Int 2014, 306573.
17. Gebhardt, R. & Hovhannisyan, A. 2010. Organ patterning in the adult stage: the role of Wnt/beta-catenin signaling in liver zonation and beyond. Dev Dyn 239, 45-55.
18. Ghionzoli, M., Repele, A., Sartiani, L., Costanzi, G., Parenti, A., Spinelli, V., David, A.L., Garriboli, M., Totonelli, G., Tian, J. et al. 2013. Human amniotic fluid stem cell differentiation along smooth muscle lineage. FASEB J 27, 4853-4865.
19. Gordeeva, O.F. 2011. Pluripotent cells in embryogenesis and in teratoma formation. J Stem Cells 6, 51-63.
20. Gordeeva, O.F. & Nikonova, T.M. 2013. Development of experimental tumors formed by mouse and human embryonic stem and teratocarcinoma cells after subcutaneous and intraperitoneal transplantations into immunodeficient and immunocompetent mice. Cell Transplant 22, 1901-1914.
21. Hashemi, S.M., Hassan, Z.M., Pourfathollah, A.A., Soudi, S., Shafiee, A. & Soleimani, M. 2013. Comparative immunomodulatory properties of adipose-derived mesenchymal stem cells conditioned media from BALB/c, C57BL/6, and DBA mouse strains. J Cell Biochem 114, 955-965.
22. Hoogduijn, M.J., Betjes, M.G. & Baan, C.C. 2014. Mesenchymal stromal cells for organ transplantation: different sources and unique characteristics? Curr Opin Organ Transplant 19, 41-46.
23. Ikegame, Y., Yamashita, K., Hayashi, S., Mizuno, H., Tawada, M., You, F., Yamada, K., Tanaka, Y., Egashira, Y., Nakashima, S., Yoshimura, S. & Iwama, T. 2011. Comparison of mesenchymal stem cells from adipose tissue and bone marrow for ischemic stroke therapy. Cytotherapy 13, 675-685.
24. Ishikawa, T., Banas, A., Hagiwara, K., Iwaguro, H. & Ochiya, T. 2010. Stem cells for hepatic regeneration: the role of adipose tissue derived mesenchymal stem cells. Curr Stem Cell Res Ther 5, 182-189.
25. Jansen, M., ten Klooster, J.P., Offerhaus, G.J. & Clevers, H. 2009. LKB1 and AMPK family signaling: the intimate link between cell polarity and energy metabolism. Physiol Rev 89, 777-798.
26. Jungermann, K. 1995. Zonation of metabolism and gene expression in liver. Histochem Cell Biol 103, 81-91.
27. Jungermann, K. & Katz, N. 1982. Functional hepatocellular heterogeneity. Hepatology 2, 385-395.
28. Jungermann, K. & Kietzmann, T. 1996. Zonation of parenchymal and nonparenchymal metabolism in liver. Annu Rev Nutr 16, 179-203.
29. Karp, J.M. & Leng Teo, G.S. 2009. Mesenchymal stem cell homing: the devil is in the details. Cell Stem Cell, 4, 206-216.
30. Kern, S., Eichler, H., Stoeve, J., Kluter, H. & Bieback, K. 2006. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 24, 1294-1301.
31. King, N.M. & Perrin, J. 2014. Ethical issues in stem cell research and therapy. Stem Cell Res Ther 5, 85.
32. Koenig, S., Aurich, H., Schneider, C., Krause, P., Haftendorn, R., Becker, H. & Christ, B. 2007. Zonal expression of hepatocytic marker enzymes during liver repopulation. Histochem Cell Biol 128, 105-114.
33. Lee, K.D., Kuo, T.K., Whang-Peng, J., Chung, Y.F., Lin, C.T., Chou, S.H., Chen, J.R., Chen, Y.P. & Lee, O.K. 2004. In vitro hepatic differentiation of human mesenchymal stem cells. Hepatology 40, 1275-1284.
34. Leibiger, C., Kosyakova, N., Mkrtchyan, H., Glei, M., Trifonov, V. & Liehr, T. 2013. First molecular cytogenetic high resolution characterization of the NIH 3T3 cell line by murine multicolor banding. J Histochem Cytochem 61, 306-312.
35. Liehr, T. & Manvelyan, M. 2009. Characterization of archived formalin-fixed/paraffin-embedded or cryofixed tissue, including nucleus extraction. In: T. Liehr (ed.) Fluorescence in situ Hybridization (FISH) - Application Guide, pp. 147-156. Springer, Berlin.
36. Liu, Y., Deng, B., Zhao, Y., Xie, S. & Nie, R. 2013. Differentiated markers in undifferentiated cells: expression of smooth muscle contractile proteins in multipotent bone marrow mesenchymal stem cells. Dev Growth Differ 55, 591-605.
37. Lotfinegad, P., Shamsasenjan, K., Movassaghpour, A., Majidi, J. & Baradaran, B. 2014. Immunomodulatory Nature and Site Specific Affinity of Mesenchymal Stem Cells: a Hope in Cell Therapy. Adv Pharm Bull 4, 5-13.
38. Marconi, S., Bonaconsa, M., Scambi, I., Squintani, G.M., Rui, W., Turano, E., Ungaro, D., D'Agostino, S., Barbieri, F., Angiari, S., Farinazzo, A., Constantin, G., del Carro, U., Bonetti, B. & Mariotti, R. 2013. Systemic treatment with adipose-derived mesenchymal stem cells ameliorates clinical and pathological features in the amyotrophic lateral sclerosis murine model. Neuroscience 248C, 333-343.
39. Meier, R.P., Muller, Y.D., Morel, P., Gonelle-Gispert, C. & Buhler, L.H. 2013. Transplantation of mesenchymal stem cells for the treatment of liver diseases, is there enough evidence? Stem Cell Res 11, 1348-1364.
40. Nishimori, M., Yakushiji, H., Mori, M., Miyamoto, T., Yaguchi, T., Ohno, S., Miyake, Y., Sakaguchi, T., Ueda, M. & Ohno, E. 2014. Tumorigenesis in cells derived from induced pluripotent stem cells. Hum Cell 27, 29-35.
41. Okita, K., Ichisaka, T. & Yamanaka, S. 2007. Generation of germline-competent induced pluripotent stem cells. Nature 448, 313-317.
42. Ong, W.K. & Sugii, S. 2013. Adipose-derived stem cells: fatty potentials for therapy. Int J Biochem Cell Biol 45, 1083-1086.
43. Pelz, S., Stock, P., Bruckner, S. & Christ, B. 2012. A methionine-choline-deficient diet elicits NASH in the immunodeficient mouse featuring a model for hepatic cell transplantation. Exp Cell Res 318, 276-287.
44. Romano, G., Morales, F., Marino, I.R. & Giordano, A. 2014. A commentary on iPS cells: potential applications in autologous transplantation, study of illnesses and drug screening. J Cell Physiol 229, 148-152.
45. Santangelo, L., Marchetti, A., Cicchini, C., Conigliaro, A., Conti, B., Mancone, C., Bonzo, J.A., Gonzalez, F.J., Alonzi, T., Amicone, L. & Tripodi, M. 2011. The stable repression of mesenchymal program is required for hepatocyte identity: a novel role for hepatocyte nuclear factor 4alpha. Hepatology 53, 2063-2074.
46. Sgodda, M., Aurich, H., Kleist, S., Aurich, I., Konig, S., Dollinger, M.M., Fleig, W.E. & Christ, B. 2007. Hepatocyte differentiation of mesenchymal stem cells from rat peritoneal adipose tissue in vitro and in vivo. Exp Cell Res 313, 2875-2886.
47. Stock, P., Bruckner, S., Ebensing, S., Hempel, M., Dollinger, M.M. & Christ, B. 2010. The generation of hepatocytes from mesenchymal stem cells and engraftment into murine liver. Nat Protoc 5, 617-627.
48. Taha, M.F. & Hedayati, V. 2010. Isolation, identification and multipotential differentiation of mouse adipose tissue-derived stem cells. Tissue Cell 42, 211-216.
49. Thompson, M.D. & Monga, S.P. 2007. WNT/beta-catenin signaling in liver health and disease. Hepatology 45, 1298-1305.
50. Wang, H., Zhao, T., Xu, F., Li, Y., Wu, M., Zhu, D., Cong, X. & Liu, Y. 2014. How important is differentiation in the therapeutic effect of mesenchymal stromal cells in liver disease? Cytotherapy 16, 309-318.
51. Yamamoto, N., Akamatsu, H., Hasegawa, S., Yamada, T., Nakata, S., Ohkuma, M., Miyachi, E., Marunouchi, T. & Matsunaga, K. 2007. Isolation of multipotent stem cells from mouse adipose tissue. J Dermatol Sci 48, 43-52.