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Hematopoietic microenvironment and the role of mesenchymal stromal cells in its organization

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Abstract

Hematopoiesis occurs in a specific microenvironment formed by the stroma of hematopoietic organs characterized by variable cellular composition. The combined action of stromal elements controls the proliferation and differentiation of hematopoietic cells by means of direct cell-cell interactions and the production of humoral factors. The role of different cell populations of transient and definitive hematopoietic organs in the maintenance of hematopoiesis, as well as the stromal mechanisms of the regulation of this process, is considered in the present review. Particular attention is paid to the contribution of mesenchymal stromal cells, which are capable both of differentiation into more specialized stromal components and direct regulation of the functioning of hematopoietic cells, to the formation of hematopoietic microenvironment.

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References

  • Aiuti, A., Cicchini, C., Bernardini, S., et al., Hematopoietic support and cytokine expression of murine-stable hepatocyte cell lines (MMH), Hepatology, 1998, vol. 28, no. 6, pp. 1645–1654.

    CAS  PubMed  Google Scholar 

  • Aizawa, S., Yaguchi, M., Nakano, M., et al., Hematopoietic supportive function of human bone marrow stromal cell lines established by a recombinant SV-40—adenovirus vector, Exp. Hematol., 1994, vol. 22, no. 6, pp. 482–487.

    CAS  PubMed  Google Scholar 

  • Arkin, S., Naparstek, B., Guarini, L., et al., Expression of intercellular adhesion molecule-1 CD54 on hematopoietic progenitors, Blood, 1991, vol. 77, no. 5, pp. 948–953.

    CAS  PubMed  Google Scholar 

  • Askmyr, M., Sims, N.A., Martin, T.J., and Purton, L.E., What is the true nature of the osteoblastic hematopoietic stem cell niche? Trends Endocrinol. Metab., 2009, vol. 20, no. 6, pp. 303–309.

    CAS  PubMed  Google Scholar 

  • Ayres-Silva, J.D., Manso, P.P., Madeira, M.R., et al., Sequential morphological characteristics of murine fetal liver hematopoietic microenvironment in Swiss Webster mice, Cell Tissue Res., 2011, vol. 344, no. 3, pp. 455–469.

    PubMed Central  Google Scholar 

  • Bensidhoum, M., Chapel, A., Francois, S., et al., Homing of in vitro expanded Stro-1− or Stro-1+ human mesenchymal stem cells into the NOD/SCID mouse and their role in supporting human CD34+ cell engraftment, Blood, 2004, vol. 103, no. 9, pp. 3313–3319.

    CAS  PubMed  Google Scholar 

  • Cain, C.J. and Manilay, J.O., Hematopoietic stem cell fate decisions are regulated by Wnt antagonists: comparisons and current controversies, Exp. Hematol., 2013, vol. 41, no. 1, pp. 3–16.

    CAS  PubMed  Google Scholar 

  • Campbell, A.D., Long, M.W., and Wicha, M.S., Developmental regulation of granulocytic cell binding to hemonectin, Blood, 1990, vol. 76, no. 9, pp. 1758–1764.

    CAS  PubMed  Google Scholar 

  • Caplan, A.I., Mesenchymal stem cells, J. Orthop. Res., 1991, vol. 9, no. 5, pp. 641–650.

    CAS  PubMed  Google Scholar 

  • Caplan, A.I., Why are MSCs therapeutic? New data: new insight, J. Pathol., 2009, vol. 217, no. 2, pp. 318–324.

    CAS  PubMed  Google Scholar 

  • Chagraoui, J., Lepage-Nolt, A., Anjo, A., et al., Fetal liver stroma consists of cells in epithelial-to-mesenchymal transition, Blood, 2003, vol. 101, no. 8, pp. 2973–2982.

    PubMed  Google Scholar 

  • Charbord, P., Oostendorp, R., Pang, W., et al., Comparative study of stromal cell lines derived from embryonic, fetal and postnatal mouse blood-forming tissues, Exp. Hematol., 2002, vol. 30, no. 10, pp. 1202–1210.

    CAS  PubMed  Google Scholar 

  • Charbord, P., Remy-Martin, J.P., Tamayo, E., et al., Analysis of the microenvironment necessary for engraftment: role of the vascular smooth muscle-like stromal cells, J. Hematother. Stem Cell Res., 2000, vol. 9, no. 6, pp. 935–943.

    CAS  PubMed  Google Scholar 

  • Chasis, J.A. and Mohandas, N., Erythroblastic islands: niches for erythropoiesis, Blood, 2008, vol. 112, no. 3, pp. 470–478.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chertkov, I.L. and Gurevich, O.A., Stvolovaya krovetvornaya kletka i ee mikrookruzhenie (Stem Hematopoietic Cell and Its Environment), Moscow: Meditsina, 1984.

    Google Scholar 

  • Chhabra, A., Lechner, A.J., Ueno, M., et al., Trophoblasts regulate the placental hematopoietic niche through PDGF-B signaling, Dev. Cell, 2012, vol. 22, no. 3, pp. 651–659.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chitteti, B.R., Cheng, Y.-H., Poteat, B., et al., Impact of interactions of cellular components of the bone marrow microenvironment on hematopoietic stem and progenitor cell function, Blood, 2010, vol. 115, no. 16, pp. 3239–3248.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chou, S. and Lodish, H.F., Fetal liver hepatic progenitors are supportive stromal cells for hematopoietic stem cells, Proc. Natl. Acad. Sci. U.S.A., 2010, vol. 107, no. 17, pp. 7799–7804.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chunmeng, S. and Tianmin, C., Effects of plastic-adherent dermal multipotent cells on peripheral blood leukocytes and CFU-GM in rats, Transplant. Proc., 2004, vol. 36, no. 5, pp. 1578–1581.

    CAS  PubMed  Google Scholar 

  • Corre, J., Barreau, C., Cousin, B., et al., Human subcutaneous adipose cells support complete differentiation but not self-renewal of hematopoietic progenitors, J. Cell. Physiol., 2006, vol. 208, no. 2, pp. 282–288.

    CAS  PubMed  Google Scholar 

  • Da Silva Meirelles, L., Chagastelles, P.C., Nardi, N.B., et al., Mesenchymal stem cells reside in virtually all postnatal organs and tissues, J. Cell Sci., 2006, vol. 119, part 11, pp. 2204–2213.

    PubMed  Google Scholar 

  • Delicat, S.E., Galvani, D.W., and Zuzel, M., A function of CD10 on bone marrow stroma, Br. J. Haematol., 1994, vol. 87, no. 3, pp. 655–657.

    Google Scholar 

  • Dennis, J.E. and Charbord, P., Origin and differentiation of human and murine stroma, Stem Cells, 2002, vol. 20, no. 3, pp. 205–214.

    CAS  PubMed  Google Scholar 

  • Diaz-Solano, D., Wittig, O., Ayala-Grosso, C., et al., Human olfactory mucosa multipotent mesenchymal stromal cells promote survival, proliferation, and differentiation of human hematopoietic cells, Stem Cells Dev., 2012, vol. 21, no. 17, pp. 3187–3196.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dzierzak, E. and Robin, C., Placenta as a source of hematopoietic stem cells, Trends Mol. Med., 2010, vol. 16, no. 8, pp. 361–367.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ehninger, A. and Trump, A., The bone marrow stem cell niche grows up: mesenchymal stem cells and macrophages move in, J. Exp. Med., 2011, vol. 208, no. 3, pp. 421–428.

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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, no. 1, pp. 95–112.

    CAS  PubMed  Google Scholar 

  • Faas, S.J., Rothstein, J.L., Kreider, B.L., et al., Phenotypically diverse mouse thymic stromal cell lines which induce proliferation and differentiation of hematopoietic cells, Eur. J. Immunol., 1993, vol. 23, no. 6, pp. 1201–1214.

    CAS  PubMed  Google Scholar 

  • Fang, B., Li, N., Song, Y., et al., Co-transplantation of haploidentical mesenchymal stem cells to enhance engraftment of hematopoietic stem cells and to reduce the risk of graft failure in two children with severe aplastic anemia, Pediatr. Transplant., 2009, vol. 13, no. 4, pp. 499–502.

    PubMed  Google Scholar 

  • Fridenshtein, A.J., Chailakhyan, R.K., and Lalykina, K.S., Fibroblast-like cells in the cultures of hematopoietic tissue of guinea pigs, Tsitologiya, 1970, vol. 12, no. 9, pp. 1147–1155.

    Google Scholar 

  • Friedenstein, A.J., Gorskaya, J.F., and Kulagina, N.N., Fibroblast precursors in normal and irradiated mouse hematopoietic organs, Exp. Hematol., 1976, vol. 4, no. 5, pp. 267–274.

    CAS  PubMed  Google Scholar 

  • Gimble, J.M., Dorheim, M.-A., Cheng, Q., et al., Adipogenesis in a murine bone marrow stromal cell line capable of supporting B lineage lymphocyte growth and proliferation: biochemical and molecular characterization, Eur. J. Immunol., 1990, vol. 20, no. 2, pp. 379–388.

    CAS  PubMed  Google Scholar 

  • Gordon, J. and Manley, N.R., Mechanisms of thymus organogenesis and morphogenesis, Development, 2011, vol. 138, no. 18, pp. 3865–3878.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gumerova, A.A. and Kiyasov, A.P., Can perisinusoidal cells be the regional stem (progenitor) cells of the liver? Kletochnaya Transplantol. Inzh., 2010, vol. 5, no. 1, pp. 33–40.

    Google Scholar 

  • Guttierrez-Ramos, J.C., Olsson, C., and Palacios, R., Interleukin (IL 1 to IL 7) gene expression in fetal liver and bone marrow stromal clones: cytokine—mediated positive and negative regulation, Exp. Hematol., 1992, vol. 20, no. 8, pp. 986–990.

    Google Scholar 

  • Haanden, J.M., Mebius, R.E., and Kraal, G., Stromal cells of the mouse spleen, Front. Immunol., 2012, vol. 3, p. 201.

    Google Scholar 

  • Han, J.Y., Goh, R.Y., Seo, S.Y., et al., Co-transplantation of cord blood hematopoietic stem cells and cultureexpanded and GM-CSF-/SCF-transfected mesenchymal stem cells in SCID mice, J. Korean Med. Sci., 2007, vol. 22, no. 2, pp. 242–247.

    PubMed Central  PubMed  Google Scholar 

  • Hangoc, G., Daub, R., Falkenburg, J.H., et al., Regulation of myelopoiesis by murine fibroblastic and adipogenic cell lines, Exp. Hematol., 1993, vol. 21, no. 4, pp. 502–505.

    CAS  PubMed  Google Scholar 

  • Hu, Y., Zhang, L.Y., Ma, G.J., et al., Phenotypical and biological characteristics of human fetal marrow and liver mesenchymal stem cells, Zhongguo Shiyan Xueyexue Zazhi, 2001, vol. 9, no. 4, pp. 289–293.

    PubMed  Google Scholar 

  • In’t Anker, P.S., Scherjon, S.A., Kleijburg-van der Keur, C., et al., Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta, Stem Cells, 2004, vol. 22, no. 7, pp. 1338–1345.

    Google Scholar 

  • Isern, J., Fraser, S.T., He, Z., and Baron, M.H., The fetal liver is a niche for maturation of primitive erythroid cells, Proc. Natl. Acad. Sci. U.S.A., 2008, vol. 105, no. 18, pp. 6662–6667.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Iwasaki, H., Arai, F., Kubota, Y., et al., Endothelial protein C receptor-expressing hematopoietic stem cells reside in the perisinusoidal niche in fetal liver, Blood, 2010, vol. 116, no. 4, pp. 544–553.

    CAS  PubMed  Google Scholar 

  • Jacobsen, K., Kravitz, J., Kincade, P.W., and Osmond, D.G., Adhesion receptor on bone marrow stromal cells: in vivo expression of vascular cell adhesion molecule—1 by reticular cells and sinusoidal endothelium in normal and γ-irradiated mice, Blood, 1996, vol. 87, no. 1, pp. 73–82.

    CAS  PubMed  Google Scholar 

  • Jelkmann, W., Regulation of erythropoietin production, J. Physiol., 2011, vol. 589, part 6, pp. 1251–1258.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kerst, J.M., Sanders, J.B., Slaper-Cortenbach, I.C.M., et al., α4β1 and α5β1 are differentially expressed during myelopoiesis and mediate the adherence of human CD34+ cells to fibronectin in an activation-dependent way, Blood, 1993, vol. 81, no. 2, pp. 344–351.

    CAS  PubMed  Google Scholar 

  • Kiel, M.J., Yilmaz, O.H., Iwashita, T., et al., SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells, Cell, 2005, vol. 121, no. 7, pp. 1109–1121.

    CAS  PubMed  Google Scholar 

  • Kierney, P.C. and Dorshkind, K., B lymphocyte precursors and myeloid progenitors survive in diffusion chamber cultures but B cell differentiation requires close association with stromal cells, Blood, 1987, vol. 70, no. 5, pp. 1418–1421.

    CAS  PubMed  Google Scholar 

  • Kim, J.A., Kang, Y.J., Park, G., et al., Identification of a stroma-mediated Wnt/beta-catenin signal promoting self-renewal of hematopoietic stem cells in the stem cell niche, Stem Cells, 2009, vol. 27, no. 6, pp. 1318–1329.

    CAS  PubMed  Google Scholar 

  • Klein, G., Müller, C.A., Tillet, E., et al., Collagen type VI in the human bone marrow microenvironment: a strong cytoadhesive component, Blood, 1995, vol. 86, no. 5, pp. 1740–1748.

    CAS  PubMed  Google Scholar 

  • Koç, O.N., Gerson, S.L., Cooper, B.W., et al., Rapid hematopoietic recovery after co-infusion of autologousblood stem cells and culture-expanded marrow mesenchymal stem cells in advanced breast cancer patients receiving high-dose chemotherapy, J. Clin. Oncol., 2000, vol. 18, no. 2, pp. 307–316.

    PubMed  Google Scholar 

  • Koenig, J.M., Ballantyne, C.M., Kumar, A.G., et al., Vascular cell adhesion molecule-1 expression and hematopoietic supportive capacity of immortalized murine stromal cell lines derived from fetal liver and adult bone marrow, In Vitro Cell. Dev. Biol. Anim., 2002, vol. 38, no. 9, pp. 538–543.

    CAS  PubMed  Google Scholar 

  • Kordes, C., Sawitza, I., Götze, S., and Häussinger, D., Hepatic stellate cells support hematopoiesis and are liver resident mesenchymal stem cells, Cell. Physiol. Biochem., 2013, vol. 31, nos. 2–3, pp. 290–304.

    CAS  PubMed  Google Scholar 

  • Lamy, I., Corlu, A., Fardel, O., et al., Rat liver biliary epithelial cells support long-term production of haemopoietic progenitors from human CD34+ cells, Br. J. Haematol., 1997, vol. 98, no. 3, pp. 560–568.

    CAS  PubMed  Google Scholar 

  • Lazarus, H.M., Koc, O.N., Devine, S.M., et al., Co-transplantation of HLA-identical sibling cultureexpanded mesenchymal stem cells and hematopoietic stem cells in hematologic malignancy patients, Biol. Blood Marrow Transplant., 2005, vol. 11, no. 5, pp. 389–398.

    PubMed  Google Scholar 

  • Lee, W.B., Erm, S.K., Kim, K.Y., and Becker, R.P., Emperipolesis of erythroblasts within Kupffer cells during hepatic hemopoiesis in human fetus, Anat. Rec., 1999, vol. 256, no. 2, pp. 158–164.

    CAS  PubMed  Google Scholar 

  • Li, D., Wang, G.Y., Liu, Z.F., et al., Macrophage-associated erythropoiesis and lymphocytopoiesis in mouse fetal liver: ultrastructural and ISH analysis, Cell Biol. Int., 2004, vol. 28, no. 6, pp. 457–461.

    CAS  PubMed  Google Scholar 

  • Li, T. and Wu, Y., Paracrine molecules of mesenchymal stem cells for hematopoietic stem cell niche, Bone Marrow Res., 2011, vol. 2011. ID 353878.

  • Li, B., Zheng, Y.W., Sano, Y., and Taniguchi, H., Evidence for mesenchymal-epithelial transition associated with mouse hepatic stem cell differentiation, PLoS One, 2011, vol. 6, no. 2, p. e17092.

    Google Scholar 

  • Linder, U., Kramer, J., Rohwedel, J., and Schlenke, P., Mesenchymal stem or stromal cells: toward a better understanding of their biology? Transfus. Med. Hemother., 2010, vol. 37, no. 2, pp. 75–83.

    Google Scholar 

  • Liu, A., Zhu, P., Li, X., et al., Ultrastructural study of the hemopoietic microenvironment in human fetal spleen, Chin. Med. Sci. J., 1994, vol. 9, no. 3, pp. 157–161.

    CAS  PubMed  Google Scholar 

  • Liu, K., Chen, Y., Zeng, Y., et al., Co-infusion of mesenchymal stromal cells facilitates platelet recovery without increasing leukemia recurrence in haploidentical hematopoietic stem cell transplantation: a randomized, controlled clinical study, Stem Cells Dev., 2011a, vol. 20, no. 10, pp. 1679–1685.

    CAS  PubMed  Google Scholar 

  • Liu, M., Yang, S.G., **ng, W., et al., Comparison of hematopoietic supportive capacity between human fetal and adult bone marrow mesenchymal stem cells in vitro, Zhongguo Shiyan Xueyexue Zazhi, 2011b, vol. 19, no. 4, pp. 1028–1032.

    CAS  PubMed  Google Scholar 

  • Long, M.W., Briddell, R., Walter, A.W., et al., Human hematopoietic stem cell adherence to cytokines and matrix molecules, J. Clin. Invest., 1992, vol. 90, no. 1, pp. 251–255.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lyman, S.D., James, L., Bos, T.V., et al., Molecular cloning of a ligand for the flt3/flk2 tyrosine kinase receptor: a proliferative factor for primitive hematopoietic cells, Cell, 1993, vol. 75, no. 6, pp. 1157–1167.

    CAS  PubMed  Google Scholar 

  • Majumdar, M.K., Thiede, M.A., Mosca, J.D., et al., Phenotypic and functional comparison of cultures of marrow-derived mesenchymal stem cells (MSCs) and stromal cells, J. Cell. Physiol., 1998, vol. 176, no. 1, pp. 57–66.

    CAS  PubMed  Google Scholar 

  • Martin, M.A. and Bhatia, M., Analysis of the human fetal liver hematopoietic microenvironment, Stem Cell Dev., 2005, vol. 14, no. 5, pp. 493–504.

    CAS  Google Scholar 

  • Mendes, S.C., Robin, C., and Dzierzak, E., Mesenchymal progenitor cells localize within hematopoietic sites throughout ontogeny, Development, 2005, vol. 132, no. 5, pp. 1127–1136.

    CAS  PubMed  Google Scholar 

  • Mendez-Ferrer, S., Michurina, T.V., Ferraro, F., et al., Mesenchymal and hematopoietic stem cells form a unique bone marrow niche, Nature, 2010, vol. 466, no. 7308, pp. 829–834.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Metcalf, D., The molecular control of cell division, differentiation commitment and maturation in hemopoietic cells, Nature, 1989, vol. 339, no. 6219, pp. 27–30.

    CAS  PubMed  Google Scholar 

  • Mikhail, A.A., Beck, E.X., Shafer, A., et al., Leptin stimulates fetal and adult erythroid and myeloid development, Blood, 1997, vol. 89, no. 5, pp. 1507–1512.

    CAS  PubMed  Google Scholar 

  • Miura, Y., Gao, Z., Miura, M., et al., Mesenchymal stem cell-organized bone marrow elements: an alternative hematopoietic progenitor resource, Stem Cells, 2006, vol. 24, no. 11, pp. 2428–2436.

    CAS  PubMed  Google Scholar 

  • Nakanishi, C., Nagaya, N., Ohnishi, S., et al., Gene and protein expression analysis of mesenchymal stem cells derived from rat adipose tissue and bone marrow, Circ. J., 2011, vol. 75, no. 9, pp. 2260–2268.

    CAS  PubMed  Google Scholar 

  • Nanno, M., Hata, M., Doi, H., et al., Stimulation of in vitro hematopoiesis by a murine fetal hepatocyte clone through cell-cell contact, J. Cell. Physiol., 1994, vol. 160, no. 3, pp. 445–454.

    CAS  PubMed  Google Scholar 

  • Naveiras, O., Nardi, V., Wenzel, P.L., et al., Bone-marrow adipocytes as negative regulators of the haematopoietic microenvironment, Nature, 2009, vol. 460, no. 7252, pp. 259–263.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nelissen, J.M., Torensma, R., Pluyter, M., et al., Molecular analysis of the hematopoiesis supporting osteoblastic cell line U2-OS, Exp. Hematol., 2000, vol. 28, no. 4, pp. 422–432.

    CAS  PubMed  Google Scholar 

  • Neves, H., Weerkamp, F., Gomes, A.C., et al., Effects of Delta1 and Jagged1 on early human hematopoiesis: correlation with expression of notch signaling-related genes in CD34+ cells, Stem Cells, 2006, vol. 24, no. 5, pp. 1328–1337.

    CAS  PubMed  Google Scholar 

  • Nishioka, K., Fujimori, Y., Hashimoto-Tamaoki, T., et al., Immortalization of bone marrow-derived human mesenchymal stem cells by removable simian virus 40T antigen gene: analysis of the ability to support expansion of cord blood hematopoietic progenitor cells, Int. J. Oncol., 2003, vol. 23, no. 4, pp. 925–932.

    CAS  PubMed  Google Scholar 

  • Ohneda, O. and Bautch, V.L., Murine endothelial cells support fetal liver erythropoiesis and myelopoiesis via distinct interactions, Br. J. Haematol., 1997, vol. 98, no. 4, pp. 798–808.

    CAS  PubMed  Google Scholar 

  • Okuyama, R., Koguma, M., Yanai, N., and Obinata, M., Bone marrow stromal cells induce myeloid and lymphoid development of the sorted hematopoietic stem cells in vitro, Blood, 1995, vol. 86, no. 7, pp. 2590–2597.

    CAS  PubMed  Google Scholar 

  • Owen, M., Marrow stromal stem cells, J. Cell Sci., 1988, suppl. 10, pp. 63–76.

    CAS  Google Scholar 

  • Payushina, O.V., Butorina, N.N., Nikonova, T.M., Kozhevnikova, M.N., Sheveleva, O.N., and Starostin, V.I., Clonal growth and differentiation of mesenchymal stromal cells from rat liver at different stages of embryogenesis, Cell Tissue Biol., 2012, vol. 6, no. 1, pp. 12–19.

    Google Scholar 

  • Payushina, O.V., Butorina, N.N., Sheveleva, O.N., et al., Mesenchymal stromal cells of the rat spleen cells in pre- and postnatal ontogenesis: a comparative analysis of clonal growth, phenotype, and differentiation potentials, Kletochnye Tekhnol. Biol. Med., 2013, no. 4, pp. 223–230.

    Google Scholar 

  • Paul, P., Rothmann, S.A., McMahon, J.T., and Gordon, A.S., Erythropoietin secretion by isolated rat Kupffer cells, Exp. Hematol., 1984, vol. 12, no. 11, pp. 825–830.

    CAS  PubMed  Google Scholar 

  • Ponomaryov, T., Peled, A., Petit, I., et al., Induction of the chemokine stromal-derived factor-1 following DNA damage improves human stem cell function, J. Clin. Invest., 2000, vol. 106, no. 11, pp. 1331–1339.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Psaila, B., Lyden, D., and Roberts, I., Megakaryocytes, malignancy and bone marrow vascular niches, J. Thromb. Haemostasis, 2012, vol. 10, no. 2, pp. 177–188.

    CAS  Google Scholar 

  • Rafii, S., Mohle, R., Shapiro, F., et al., Regulation of hematopoiesis by microvascular endothelium, Leuk. Lymphoma, 1997, vol. 27, nos. 5–6, pp. 375–386.

    CAS  PubMed  Google Scholar 

  • Robin, C., Bollerot, K., Mendes, S., et al., Human placenta is a potent hematopoietic niche containing hematopoietic stem and progenitor cells throughout development, Cell Stem Cell, 2009, vol. 5, no. 4, pp. 385–395.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rogers, J.A. and Berman, J.W., Tumor necrosis factor–responsive long-term–culture-initiating cell is associated with the stromal layer of mouse long-term bone marrow cultures, Proc. Natl. Acad. Sci. U.S.A., 1993, vol. 10, no. 12, pp. 5777–5780.

    Google Scholar 

  • Ruoslahti, E. and Yamaguchi, Y., Proteoglycans as mediators of growth factor activities, Cell, 1991, vol. 64, no. 5, pp. 867–869.

    CAS  PubMed  Google Scholar 

  • Sadlon, T.J., Lewis, I.D., and D’Andrea, R.J., BMP4: its role in development of the hematopoietic system and potential as a hematopoietic growth factor, Stem Cells, 2004, vol. 22, no. 4, pp. 457–474.

    CAS  PubMed  Google Scholar 

  • Sakai, T., Ohta, M., Kawakatsu, H., et al., Tenascin-C induction in Whitlock-Witte culture: a relevant role of the thiol moiety in lymphoid-lineage differentiation, Exp. Cell Res., 1995, vol. 217, no. 2, pp. 395–403.

    CAS  PubMed  Google Scholar 

  • Seki, M., Kameoka, J., Takahashi, S., et al., Identification of tenascin-C as a key molecule determining stromal cell-dependent erythropoiesis, Exp. Hematol., 2006, vol. 34, no. 4, pp. 519–527.

    CAS  PubMed  Google Scholar 

  • Sensebe, L., Deschaseaux, M., Li, J., et al., The broad spectrum of cytokine gene expression by myoid cells from the human marrow microenvironment, Stem Cells, 1997, vol. 15, no. 2, pp. 133–143.

    CAS  PubMed  Google Scholar 

  • Seshi, B., Kumar, S., and Sellers, D., Human bone marrow stromal cell: co-expression of markers specific for multiple mesenchymal cell lineages, Blood Cells Mol. Dis., 2000, vol. 26, no. 3, pp. 234–246.

    CAS  PubMed  Google Scholar 

  • Signore, M., Cerio, A.M., Boe, A., et al., Identity and ranking of colonic mesenchymal stromal cells, J. Cell Physiol., 2012, vol. 227, no. 9, pp. 3291–3300.

    CAS  PubMed  Google Scholar 

  • Siler, U., Seiffert, M., Puch, S., et al., Characterization and functional analysis of laminin isoforms in human bone marrow, Blood, 2000, vol. 96, no. 13, pp. 4194–4203.

    CAS  PubMed  Google Scholar 

  • Sugimoto, A., Yamamoto, M.., Suzuki, M., et al., Delta-4 Notch ligand promotes erythroid differentiation of human umbilical cord blood CD34+ cells, Exp. Hematol., 2006, vol. 34, no. 4, pp. 424–432.

    CAS  PubMed  Google Scholar 

  • Sugiyama, D., Inoue-Yokoo, T., Fraser, S.T., et al., Embryonic regulation of the mouse hematopoietic niche, Sci. World J., 2011a, vol. 11, pp. 1770–1780.

    CAS  Google Scholar 

  • Sugiyama, D., Kulkeaw, K., Mizuochi, C., et al., Hepatoblasts comprise a niche for fetal liver erythropoiesis through cytokine production, Biochem. Biophys. Res. Commun., 2011b, vol. 410, no. 2, pp. 301–306.

    CAS  PubMed  Google Scholar 

  • Sugiyama, T. and Nagasawa, T., Bone marrow niches for hematopoietic stem cells and immune cells, Inflammatory Allergy Drug Targets, 2012, vol. 11, no. 3, pp. 201–206.

    CAS  Google Scholar 

  • Suniara, R.K., Jenkinson, E.J., and Owen, J.J., An essential role for thymic mesenchyme in early T cell development, J. Exp. Med., 2000, vol. 191, no. 6, pp. 1051–1056.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tamiolakis, D., Venizelos, I., Nikolaidou, S., and Jivanakis, T., Normal development of fetal hepatic haematopoiesis during the second trimester of gestation is upregulated by fibronectin expression in the stromal cells of the portal triads, Rev. Esp. Enferm. Dig., 2007, vol. 99, no. 10, pp. 576–580.

    CAS  PubMed  Google Scholar 

  • Timens, W. and Kamps, W.A., Hemopoiesis in human fetal and embryonic liver, Microsc. Res. Tech., 1997, vol. 39, no. 5, pp. 387–397.

    CAS  PubMed  Google Scholar 

  • Toksoz, D., Zsebo, K.M., Smith, K.A., et al., Support of human hematopoiesis in long-term bone marrow cultures by murine stromal cells selectively expressing the membrane-bound and secreted forms of the human homolog of the steel gene product, stem cell factor, Proc. Natl. Acad. Sci. U.S.A., 1992, vol. 89, no. 16, pp. 7350–7354.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tsuchiyama, J., Mori, M., and Okada, S., Murine spleen stromal cell line SPY3-2 maintains long-term hematopoiesis in vitro, Blood, 1995, vol. 85, no. 11, pp. 3107–3116.

    CAS  PubMed  Google Scholar 

  • Ulyanova, T., Scott, L.M., Priestley, G.V., et al., VCAM-1 expression in adult hematopoietic and nonhematopoietic cells is controlled by tissue-inductive signals and reflects their developmental origin, Blood, 2005, vol. 106, no. 1, pp. 86–94.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Vacanti, V., Kong, E., Suzuki, G., et al., Phenotypic changes of adult porcine mesenchymal stem cells induced by prolonged passaging in culture, J. Cell. Physiol., 2005, vol. 205, pp. 194–201.

    CAS  PubMed  Google Scholar 

  • Van Den Berg, D.J., Sharma, A.K., Bruno, E., and Hoffman, R., Role of members of the Wnt gene family in human hematopoiesis, Blood, 1998, vol. 92, no. 9, pp. 3189–3202.

    Google Scholar 

  • Van Den Heuvel, R.L., Versele, S.R.M., Schoeters, G.E.R., and Vanderborght, O.L.J., Stromal stem cells (CFU-F) in yolk sac, liver, spleen and bone marrow of pre- and postnatal mice, Br. J. Haematol., 1987, vol. 66, no. 1, pp. 15–20.

    PubMed  Google Scholar 

  • 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, no. 6, pp. 488–493.

    PubMed  Google Scholar 

  • Wagner, W., Roderburg, C., Wein, F., et al., Molecular and secretory profiles of human mesenchymal stromal cells and their abilities to maintain primitive hematopoietic progenitors, Stem Cells, 2007, vol. 25, no. 10, pp. 2638–2647.

    CAS  PubMed  Google Scholar 

  • Wallace, S.R., Oken, M.M., Lunetta, K.L., et al., Abnormalities of bone marrow mesenchymal cells in multiple myeloma patients, Cancer, 2001, vol. 91, no. 7, pp. 1219–1230.

    CAS  PubMed  Google Scholar 

  • Wang, X.Y., Lan, Y., He, W.Y., et al., Identification of mesenchymal stem cells in aorta-gonad-mesonephros and yolk sac of human embryos, Blood, 2008, vol. 111, no. 4, pp. 2436–2443.

    CAS  PubMed  Google Scholar 

  • Wang, X.Y., Liu, B., Yuan, C.H., et al., Effect of bone marrow mesenchymal stem cells on hematopoietic differentiation of murine embryonic stem cells, Zhongguo Shiyan Xueyexue Zazhi, 2003, vol. 11, no. 4, pp. 329–334.

    PubMed  Google Scholar 

  • Wang, H., Wang, Z., Zheng, X., et al., Hematopoietic stem cell transplantation with umbilical cord multipotent stromal cell infusion for the treatment of aplastic anemia–a single-center experience, Cytotherapy, 2013, vol. 15, no. 9, pp. 1118–1125.

    CAS  PubMed  Google Scholar 

  • Weinstein, R., Riordan, M.A., Wenc, K., et al., Dual role of fibronectin in hematopoietic differentiation, Blood, 1989, vol. 73, no. 1, pp. 111–116.

    CAS  PubMed  Google Scholar 

  • Wineman, J., Moore, K., Lemischka, I., and Muller-Sieburg, C., Functional heterogeneity of the hematopoietic microenvironment: rare stromal elements maintain long-term repopulating stem cell, Blood, 1996, vol. 87, no. 10, pp. 4082–4090.

    CAS  PubMed  Google Scholar 

  • Wittig, O., Paez-Cortez, J., and Cardier, J.E., Liver sinusoidal endothelial cells promote B lymphopoiesis from primitive hematopoietic cells, Stem Cells Dev., 2010, vol. 19, no. 3, pp. 341–350.

    CAS  PubMed  Google Scholar 

  • Wolf, N.S., Bertoncello, I., Jiang, D., and Priestley, G., Developmental hematopoiesis from prenatal to youngadult life in the mouse model, Exp. Hematol., 1995, vol. 23, no. 2, pp. 142–146.

    CAS  PubMed  Google Scholar 

  • Yin, T. and Li, L., The stem cell niches in bone, J. Clin. Invest., 2006, vol. 116, no. 5, pp. 1195–1201.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang, H., Miao, Z., He, Z., et al., The existence of epithelial-to-mesenchymal cells with the ability to support hematopoiesis in human fetal liver, Cell. Biol. Int., 2005, vol. 29, no. 3, pp. 213–219.

    CAS  PubMed  Google Scholar 

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  1. Kol’tsov Institute of Developmental Biology, Russian Academy of Sciences, ul. Vavilova 26, Moscow, 119334, Russia

    O. V. Payushina

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Original Russian Text © O.V. Payushina, 2015, published in Uspekhi Sovremennoi Biologii, 2015, Vol. 135, No. 1, pp. 52–63.

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Payushina, O.V. Hematopoietic microenvironment and the role of mesenchymal stromal cells in its organization. Biol Bull Rev 5, 383–393 (2015). https://doi.org/10.1134/S207908641504009X

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