Abstract
Fetal liver, during its hematopoietic activity, contains mesenchymal stromal cells (MSCs) generating its hematopoietic microenvironment. These cells are clonogenic and capable of multilineage differentiation; however, little is known about how their properties alter during embryogenesis. We compared the cloning efficiency of MSCs from rat fetal liver at 14, 16, and 20 days of development, as well as their capacity for osteo- and adipogenesis in vitro and chondrogenesis in vivo by ectopic transplantation of intact liver. The relative content of clonogenic MSCs in liver cell suspension was highest in 16-day fetuses and lowest in 20-day fetuses. Cells from 14-day fetuses exhibited high osteogenic and less apparent adipogenic and chondrogenic potential; cells from 20-day fetuses displayed weak adipogenic capacity and no osteo- or chondrogenic ability. These results show the correlation of MSC content and the cell differentiation potential with hematopoietic dynamics in developing rat liver. It may be thought that the changes we observed are related to the loss of hematopoietic activity and liver getting of definitive functions.
Similar content being viewed by others
Abbreviations
- CFU-F:
-
colony forming units of fibroblasts
- MSC:
-
mesenchymal stromal cells
- AP:
-
alkaline phophatase
References
Abramoff, M.D., Magelhaes, P.J., and Ram, S.J., Image Processing with ImageJ, Biophoton. Int., 2004, vol. 11, pp. 36–42.
Aiuti, A., Cicchini, C., Bernardini, S., Fedele, G., Amicone, L., Fantoni, A., and Tripodi, M., Hematopoietic Support and Cytokine Expression of Murine-Stable Hepatocyte Cell Lines (MMH), Hepatology, 1998, vol. 28, pp. 1645–1654.
Corlu, A., Lamy, I., Ilyin, G.P., Fardel, O., Kneip, B., Le, Jossic, C., and Guguen-Guillouzo, C., Hematopoiesis-Promoting Activity of Rat Liver Biliary Epithelial Cells: Involvement of a Cell Surface Molecule, Liver-Regulating Protein, Exp. Hematol., 1998, vol. 26, pp. 382–394.
Emura, I., Sekiya, M., and Ohnishi, Y., Ultrastructural Identification of the Hemopoietic Inductive Microenvironment in the Human Embryonic Liver, Arch. Histol. Jpn., 1984, vol. 47, pp. 95–112.
Fridenshtein, A.Ya. and Luriya, E.A., Kletochnye osnovy krovetvornogo mikrookruzheniya (Cellular Basis of Hematopoietic Microenvironment), Moscow: Meditsina, 1980.
Fridenshtein, A.Ya., Chaylakhyan, R.K., and Lalykina, K.S., O Fibroblast-Like Cells in Cultures of Guinea Pig Hematopoietic Tissue, Tsitologiia, 1970, vol. 12, no. 9, pp. 1147–1155.
Fromigue, O., Hamidouche, Z., Chateauvieux, S., Charbord, P., and Marie, P.J., Distinct Osteoblastic Differentiation of Murine Fetal Liver and Bone Marrow Stromaderived Mesenchymal Stem Cells, J. Cell Biochem., 2008, vol. 104, pp. 620–628.
Fukumoto, T., Possible Developmental Interactions of Hematopoietic Cells and Hepatocytes in Fetal rat Liver, Biomed. Res., 1992, vol. 13, pp. 385–413.
Götherström, C., Ringden, O., Westgren, M., Tammik, C., and Le, Blanc, K., Immunomodulatory Effects of Human Foetal Liver-Derived Mesenchymal Stem Cells, Bone Marrow Transplant, 2003, vol. 32, pp. 265–272.
Guillot, P.V., Gotherstrom, C., Chan, J., Kurata, H., and Fisk, N.M., Human First-trimester Fetal MSC Express Pluripotency Markers and Grow Faster and Have Longer Telomeres than Adult MSC, Stem Cells, 2007, vol. 25, pp. 646–654.
Guo, Y., Zhang, X., Huang, J., Zeng, Y., Liu, W., Geng, C., Li, K.W., Yang, D., Wu, S., Wei, H., Han, Z., Qian, X., Jiang, Y., and He, F., Relationships between Hematopoiesis and Hepatogenesis in the Midtrimester Fetal Liver Characterized by Dynamic Transcriptomic and Proteomic Profiles, PLoS ONE, 2009, vol. 4, p. e7641.
in’t Anker, P., Noort, W.A., Scherjon, S.A., Kleijburg-van, der, Keur, C., Kruisselbrink, A.B., Bezooijen, R.L., Beekhuizen, W., Willemze, R., Kanhai, H., and Fibbe, W.E., Mesenchymal Stem Cells in Human Second-Trimester Bone Marrow, Liver, Lung and Spleen Exhibit a Similar Immunophenotype but a Heterogeneous Multilineage Differentiation Potential, Haematologica, 2003, vol. 88, pp. 845–852.
Kozhevnikova, M.N., Mikaelyan, A.S., and Starostin, V.I., Molecular Genetic and Immunophenotypic Analysis of Antigen Profiling, Osteogenic and Adipogenic Potentials of Mesenchymal Stromal Cells from Fetal Liver and Adult Bone Marrow in Rats, Tsitologiia, 2009, vol. 51, no. 6, pp. 526–538.
Majumdar, M.K., Thiede, M.A., Haynesworth, S.E., Bruder, S.P., and Gerson, S.L., Human Marrow-Derived Mesenchymal Stem Cells (MSCs) Express Hematopoietic Cytokines and Support Long-Term Hematopoiesis when Differentiated toward Stromal and Osteogenic Lineages, J. Hematother. Stem Cell Res., 2000, vol. 9, pp. 841–848.
Majumdar, M.K., Thiede, M.A., Mosca, J.D., Moorman, M., and Gerson, S.L., Phenotypic and Functional Comparison of Cultures of Marrow-Derived Mesenchymal Stem Cells (MSCs) and Stromal Cells, J. Cell. Physiol., 1998, vol. 176, pp. 57–66.
Nanno, M., Hata, M., Doi, H., Satomi, S., Yagi, H., Sakata, T., Suzuki, R., and Itoh, T., Stimulation of in vitro Hematopoiesis by a Murine Fetal Hepatocyte Clone through Cell-Cell Contact, J. Cell. Physiol., 1994, vol. 160, pp. 445–454.
Payushina, O.V., Bueverova, E.I., Satdykova, G.P., Starostin, V.I., Domaratskaya, E.I., and Khruschov, N.G., Comparative Investigation of Mesenchymal Stem Cells Isolated from the Bone Marrow and Embryonic Liver of Mouse and Rat, Biol. Bull., 2004, vol. 31, no. 6, pp. 546–551.
Pirs, E., Gistokhimiya (Histochemistry), Moscow: Inostr. Liter., 1962.
Ryden, M., Dicker, A., Götherström, C., Aström, G., Tammik, C., Arner, P., and Le, Blanc, K., Functional Characterization of Human Mesenchymal Stem Cell-Derived Adipocytes, Biochem. Biophys. Rec. Commun., 2003, vol. 311, pp. 391–397.
Sasaki, K., and Sonoda, Y., Histometrical and Three-Dimensional Analyses of Liver Hematopoiesis in the Mouse Embryo, Arch. Histol. Cytol., 2000, vol. 63, pp. 137–146.
Starostin, V.I., and Domaratskaya, E.I., Chondrogenesis and Osteogenesis in Ectopic Transplants of the Fetal Liver in Mice, Russ. J. Dev. Biol., 2001, vol. 32, no. 2, pp. 88–91.
Strelkov, R.B., Tablitsy Strelkova i ekspress-metod statisticheskoy obrabotki dannykh (Strelkov’s Tables and Rapid Method of Statistical Data Processing), Moscow: PAIMS, 1999.
Van Den Heuvel, R., Mathieu, E., Schoeters, G.E.R., Leppens, H., and Vanderborght, O.L., Stromal Cells from Murine Developing Hemopoietic Organs: Comparison of Colony-Forming Unit of Fibroblasts and Long-Term Cultures, Int. J. Dev. Biol., 1991, vol. 35, pp. 33–41.
Van Den Heuvel, R.L., Versele, S.R.M., Schoeters, G.E.R., and Vanderborght, O.L., Stromal Stem Cells (CFU-F) in Yolk Sac, Liver, Spleen and Bone Marrow of Pre- and Postnatal Mice, Br. J. Haematol., 1987, vol. 66, pp. 15–20.
Van Overstraeten-Schlögel, N., Beguin, Y., and Gothot, A., Role of Stromal-Derived Factor-1 in the Hematopoietic-Supporting Activity of Human Mesenchymal Stem Cells, Eur. J. Haematol., 2006, vol. 76, pp. 488–493.
Versele, S.R., Van, Den, Heuvel, R.L., Schoeters, G.E.R., and Vanderborght, O.L.., Proliferation Activity of Stromal Stem Cells (CFU-f) from Hemopoietic Organs of Pre- and Postnatal Mice, Radiat. Res., 1987, vol. 111, pp. 185–191.
Wang, J., Zhou, J., and Zhao, Z., Experimental Study of Osteogenic Induction of Fetal Mouse Liver Mesenchymal Stem Cells in vitro and Their Biologic Attachment Properties to True Bone Ceramic, Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi, 2005, vol. 19, pp. 648–651.
Wolf, N.S., Bertoncello, I., Jiang, D., and Priestley, G., Developmental Hematopoiesis from Prenatal to Young-Adult life in the Mouse Model, Exp. Hematol., 1995, vol. 23, pp. 142–146.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © O.V. Payushina, N.N. Butorina, T.M. Nikonova, M.N. Kozhevnikova, O.N. Sheveleva, V.I. Starostin, 2011, published in Tsitologiya, 2011, Vol. 53, No. 11, pp. 859–867.
Rights and permissions
About this article
Cite this article
Payushina, O.V., Butorina, N.N., Nikonova, T.M. et al. Clonal growth and differentiation of mesenchymal stromal cells from rat liver at different stages of embryogenesis. Cell Tiss. Biol. 6, 12–19 (2012). https://doi.org/10.1134/S1990519X12010075
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1990519X12010075