Skip to main content
SpringerLink
Log in

Localization and functions of mesenchymal stromal cells in vivo

  • Published:
Biology Bulletin Reviews Aims and scope Submit manuscript

Abstract

The study of mesenchymal stromal cells (MSCs) is a very topical problem. Numerous experiments in vitro advanced the understanding of MSC biology to a great extent. However, many aspects of their behavior in vivo still remain unclear. This review deals with MSC localization and functioning in an organism. MSCs are present in various tissues, changing their numbers and traits during ontogenesis. Pericytes, or adventitial cells, can be considered possible equivalents of MSCs in vivo. Self-maintenance, proliferation, and differentiation of MSCs are controlled by their tissue microenvironment, which includes the surrounding cells, soluble molecules, and extracellular matrix. At early stages of ontogenesis, MSCs probably migrate throughout an organism and populate various tissues. The migration occurs also through a mature organism when tissues happen to be damaged. MSCs move pointedly to the damaged parts and render a reparative effect that is due primarily to the paracrine production of bioactive molecules and immunomodulatory properties of MSCs rather than their differentiation. An important function of MSCs is the creation of hematopoietic microenvironment by the secretion of cytokines and chemoattractants, as well as by direct interaction with hemopoietic cells. It is possible that MSCs sustain the stable functioning of not only hematopoietic but also other tissues. Their unique features make them quite attractive for clinical use, although the successful introduction of MSC into medical practice requires further study of their interaction with the recipient organism and their effect on regeneration.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aoki, S., Toda, S., Ando, T., and Sugihara, H., Bone marrow stromal cells, preadipocytes, and dermal fibroblasts promote epidermal regeneration in their distinctive fashions, Mol. Biol. Cell., 2004, vol. 15, pp. 4647–4657.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Baksh, D., Davies, J.E., and Zandstra, P.W., Soluble factor cross-talk between human bone marrow-derived hematopoietic and mesenchymal cells enhances in vitro CFU-F and CFU-O growth and reveals heterogeneity in the mesenchymal progenitor cell compartment, Blood, 2005, vol. 106, no. 9, pp. 3012–3019.

    Article  CAS  PubMed  Google Scholar 

  • Baksh, D., Song, L., and Tuan, R.S., Adult mesenchymal stem cells: characterization, differentiation, and application in cell and gene therapy, J. Cell. Mol. Med., 2004, vol. 8, no. 3, pp. 301–316.

    Article  CAS  PubMed  Google Scholar 

  • Ball, S.G., Shuttleworth, A.C., and Kielty, C.M., Direct cell contact influences bone marrow mesenchymal stem cell fate, Int. J. Biochem. Cell Biol., 2004, vol. 36, no. 4, pp. 714–727.

    Article  CAS  PubMed  Google Scholar 

  • Baraniak, P.R. and McDevitt, T.C., Scaffold-free culture of mesenchymal stem cell spheroids in suspension preserves multilineage potential, Cell Tissue Res., 2012, vol. 347, no. 3, pp. 701–711.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bellows, C.G., Pei, W., Jia, Y., and Heersche, J.N., Proliferation, differentiation and self-renewal of osteoprogenitors in vertebral cell populations from aged and young female rats, Mech. Ageing Dev., 2003, vol. 124, no. 6, pp. 747–757.

    Article  CAS  PubMed  Google Scholar 

  • Benayahu, D., Akavia, U.D., and Shur, I., Differentiation of bone marrow stroma-derived mesenchymal cells, Curr. Med. Chem., 2007, vol. 14, no. 2, pp. 173–179.

    Article  CAS  PubMed  Google Scholar 

  • Bernardo, M.E., Emons, J.A., Karperien, M., Nauta, A.J., Willemze, R., Roelofs, H., Romeo, S., Marchini, A., Rappold, G.A., Vukicevic, S., Locatelli, F., and Fibbe, W.E., Human mesenchymal stem cells derived from bone marrow display a better chondrogenic differentiation compared with other sources, Connect. Tissue Res., 2007, vol. 48, no. 3, pp. 132–140.

    Article  CAS  PubMed  Google Scholar 

  • Bui, K.C., Senadheera, D., Wang, X., Hendrickson, B., Friedlich, P., and Lutzko, C., Recovery of multipotent progenitors from the peripheral blood of patients requiring extracorporeal membrane oxygenation support, Am. J. Respir. Crit. Care Med., 2010, vol. 181, no. 3, pp. 226–237.

    Article  PubMed  Google Scholar 

  • Buravkova, L.B., Andreeva, E.R., and Grigoriev, A.I., The impact of oxygen in physiological regulation of human multipotent mesenchymal cell functions, Hum. Physiol., 2012, vol. 38, no. 4, pp. 444–452.

    Article  CAS  Google Scholar 

  • Caplan, A.I., All MSCs are pericytes? Cell Stem Cell., 2008, vol. 3, no. 3, pp. 229–230.

    Article  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.

    Article  CAS  PubMed  Google Scholar 

  • Chang, C.P., Chio, C.C., Cheong, C.U., Chao, C.M., Cheng, B.C., and Lin, M.T., Hypoxic preconditioning enhances the therapeutic potential of the secretome from cultured human mesenchymal stem cells in experimental traumatic brain injury, Clin. Sci., 2013, vol. 124, no. 3, pp. 165–176.

    Article  CAS  PubMed  Google Scholar 

  • Chen, X.-D., Dusevich, V., Feng, J.Q., Manolagas, S.C., and Jilka, R.L., Extracellular matrix made by bone marrow cells facilitates expansion of marrow-derived mesenchymal progenitor cells and prevents their differentiation into osteoblasts, J. Bone Miner. Res., 2007, vol. 22, no. 12, pp. 1943–1956.

    Article  CAS  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.

    Article  CAS  PubMed  Google Scholar 

  • Corselli, M., Chen, C.-W., Crisan, M., Lazzari, L., and Péault, B., Perivascular ancestors of adult multipotent stem cells, Arterioscler., Thromb., Vasc. Biol., 2010, vol. 30, no. 6, pp. 1104–1109.

    Article  CAS  Google Scholar 

  • Covas, D.T., Panepucci, R.A., Fontes, A.M., Silva, W.A., Jr., Orellana, M.D., Freitas, M.C.C., Neder, L., Santos, A.R.D., Peres, L.C., Jamur, M.C., and Zago, M.A., Multipotent mesenchymal stromal cells obtained from diverse human tissues share functional properties and gene-expression profile with CD146+ perivascular cells and fibroblasts, Exp. Hematol., 2008, vol. 36, no. 5, pp. 642–654.

    Article  CAS  PubMed  Google Scholar 

  • Curley, G.F., Hayes, M., Ansari, B., Shaw, G., Ryan, A., Barry, F., O’Brien, T., O’Toole, D., and Laffey, J.G., Mesenchymal stem cells enhance recovery and repair following ventilator-induced lung injury in the rat, Thorax, 2012, vol. 67, no. 6, pp. 496–501.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  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.

    Article  CAS  PubMed  Google Scholar 

  • Diaz-Solano, D., Wittig, O., Ayala-Grosso, C., Pieruzzini, R., and Cardier, J.E., 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Djouad, F., Delorme, B., Maurice, M., Bony, C., Apparailly, F., Louis-Plence, P., Canovas, F., Charbord, P., Noël, D., and Jorgensen, C., Microenvironmental changes during differentiation of mesenchymal stem cells toward chondrocytes, Arthritis Res. Ther., 2007, vol. 9, no. 2, p. R33.

    Google Scholar 

  • Docheva, D., Popov, C., Mutschler, W., and Schieker, M., Human mesenchymal stem cells in contact with their environment: surface characteristics and the integrin system, J. Cell. Mol. Med., 2007, vol. 11, no. 1, pp. 21–38.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dominici, M., Le Blanc, K., Mueller, I., Slaper-Cortenbach, I., Marini, F., Krause, D., Deans, R., Keating, A., Prockop, D., and Horwitz, E., Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement, Cytotherapy, 2006, vol. 8, no. 4, pp. 315–317.

    Article  CAS  PubMed  Google Scholar 

  • Dwyer, R.M., Potter-Beirne, S.M., Harrington, K.A., Lowery, A.J., Hennessy, E., Murphy, J.M., Barry, F.P., O’Brien, T., and Kerin, M.J., Monocyte chemotactic protein-1 secreted by primary breast tumors stimulates migration of mesenchymal stem cells, Clin. Cancer Res., 2007, vol. 13, no. 17, pp. 5020–5027.

    Article  CAS  PubMed  Google Scholar 

  • Ehninger, A. and Trumpp, 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.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fouraschen, S.M., Pan, Q., de Ruiter, P.E., Farid, W.R., Kazemier, G., Kwekkeboom, J., Ijzermans, J.N., Metselaar, H.J., Tilanus, H.W., de Jonge, J., and van der Laan, L.J., Secreted factors of human liver-derived mesenchymal stem cells promote liver regeneration early after partial hepatectomy, Stem Cells Dev., 2012, vol. 21, no. 13, pp. 2410–2419.

    Article  CAS  PubMed  Google Scholar 

  • Fridenstein, A.Ya., Chailakhyan, R.K., and Lalykina, K.S., About fibroblast-like cells of hemopoietic tissue of guinea pigs in vitro, 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 

  • Ghilzon, R., McCulloch, C.A., and Zohar, R., Stromal mesenchymal progenitor cells, Leuk. Lymphoma, 1999, vol. 32, nos. 3-4, pp. 211–221.

    CAS  PubMed  Google Scholar 

  • Gordon, M.Y., Extracellular matrix of the marrow microenvironment, Br. J. Haematol., 1988, vol. 70, no. 1, pp. 1–4.

    Article  CAS  PubMed  Google Scholar 

  • 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, no. 3, pp. 646–654.

    Article  CAS  PubMed  Google Scholar 

  • Han, J.Y., Goh, R.Y., Seo, S.Y., Hwang, T.H., Kwon, H.C., Kim, S.H., Kim, J.S., Kim, H.J., and Lee, Y.H., Cotransplantation of cord blood hematopoietic stem cells and culture-expanded and GM-CSF-/SCF-transfected mesenchymal stem cells in SCID mice, J. Korean Med. Sci., 2007, vol. 22, no. 2, pp. 242–247.

    Article  PubMed Central  PubMed  Google Scholar 

  • Haniffa M.A., Collin, M.P., Buckley, C.D., and Dazzi, F., Mesenchymal stem cells: the fibroblast’s new clothes? Haematologica, 2009, vol. 94, no. 2, pp. 258–263.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hegyi, B., Sági, B., Kovács, J., Kiss, J., Urbán, V.S., Mészáros, G., Monostori, E., and Uher, F., Identical, similar or different? Learning about immunomodulatory function of mesenchymal stem cells isolated from various mouse tissues: bone marrow, spleen, thymus, and aorta wall, Int. Immunol., 2010, vol. 22, no. 7, pp. 551–559.

    Article  CAS  PubMed  Google Scholar 

  • Heino, T.J., Alm, J.J., Moritz, N., and Aro, H.T., Comparison of the osteogenic capacity of minipig and human bone marrow-derived mesenchymal stem cells, J. Orthop. Res., 2012, vol. 30, no. 7, pp. 1019–1025.

    Article  PubMed  Google Scholar 

  • Heino, T.J., Hentunen, T.A., and Vaananen, H.K., Conditioned medium from osteocytes stimulates the proliferation of bone marrow mesenchymal stem cells and their differentiation into osteoblasts, Exp. Cell Res., 2004, vol. 294, no. 2, pp. 458–468.

    Article  CAS  PubMed  Google Scholar 

  • Heuvel van den, 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 preand postnatal mice, Br. J. Haematol., 1987, vol. 66, no. 1, pp. 15–20.

    Article  Google Scholar 

  • Horwitz, E.M., Prockop, D.J., Fitzpatrick, L.A., Koo, W.W., Gordon, P.L., Neel, M., Sussman, M., Orchard, P., Marx, J.C., Pyeritz, R.E., and Brenner, M.K., Transplantability and therapeutic effects of bone marrowderived mesenchymal cells in children with osteogenesis imperfecta, Nat. Med., 1999, vol. 5, no. 3, pp. 309–313.

    Article  CAS  PubMed  Google Scholar 

  • Hu, Y., Liao, L., Wang, Q., Ma, L., Ma, G., Jiang, X., and Zhao, R.C., Isolation and identification of mesenchymal stem cells from human fetal pancreas, J. Lab. Clin. Med., 2003, vol. 141, no. 5, pp. 342–349.

    Article  CAS  PubMed  Google Scholar 

  • Hu, C., Yong, X., Li, C., Lü, M., Liu, D., Chen, L., Hu, J., Teng, M., Zhang, D., Fan, Y., and Liang, G., CXCL12/CXCR4 axis promotes mesenchymal stem cell mobilization to burn wounds and contributes to wound repair, J. Surg. Red., 2013, vol. 183, no. 1, pp. 427–434.

    Article  CAS  Google Scholar 

  • Huang, Y., Chen, P., Zhang, C.B., Ko, G.J., Ruiz, M., Fiorina, P., Hussain, M.A., Wasowska, B.A., Rabb, H., and Womer, K.L., Kidney-derived mesenchymal stromal cells modulate dendritic cell function to suppress alloimmune responses and delay allograft rejection, Transplantation, 2010, vol. 90, no. 12, pp. 1307–1311.

    Article  CAS  PubMed  Google Scholar 

  • In’t Anker, P.S., Noort, W.A., Scherjon, S.A., Kleijburg van der Keur, C., Kruisselbrink, A.B., van Bezooijen, R.L., Beekhuizen, W., Willemze, R., Kanhai, H.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, J. Hematol., 2003, vol. 88, no. 8, pp. 845–852.

    Google Scholar 

  • In’t Anker, P.S., Scherjon, S.A., Kleijburg van der Keur, C., de Groot-Swings, G.M., Claas, F.H., Fibbe, W.E., and Kanhai, H.H., Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta, Stem Cells, 2004, vol. 22, no. 7, pp. 1338–1345.

    Article  Google Scholar 

  • Iso, Y., Spees, J.L., Serrano, C., Bakondi, B., Pochampally, R., Song, Y.H., Sobel, B.E., Delafontaine, P., and Prockop, D.J., Multipotent human stromal cells improve cardiac function after myocardial infarction in mice without long-term engraftment, Biochem. Biophys. Res. Commun., 2007, vol. 354, no. 3, pp. 700–706.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Isoda, K., Kojima, M., Takeda, M., Higashiyama, S., Kawase, M., and Yagi, K., Maintenance of hepatocyte functions by co-culture with bone marrow stromal cells, J. Biosci. Bioeng., 2004, vol. 97, no. 5, pp. 343–346.

    Article  CAS  PubMed  Google Scholar 

  • Jones, E. and McGonagle, D., Human bone marrow mesenchymal stem cells in vivo, Rheumatology, 2008, vol. 47, no. 2, pp. 126–131.

    Article  CAS  PubMed  Google Scholar 

  • Kinnaird, T., Stabile, E., Burnett, M.S., Shou, M., Lee, C.W., Barr, S., Fuchs, S., and Epstein, S.E., Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms, Circulation, 2004, vol. 109, no. 12, pp. 1543–1549.

    Article  CAS  PubMed  Google Scholar 

  • Koerner, J., Nesic, D., Romero, J.D., Brehm, W., MainilVarlet, P., and Grogan, S.P., Equine peripheral bloodderived progenitors in comparison to bone marrowderived mesenchymal stem cells, Stem Cells, 2006, vol. 24, no. 6, pp. 1613–1619.

    Article  CAS  PubMed  Google Scholar 

  • Kolf, C.M., Cho, E., and Tuan, R.S., Biology of adult mesenchymal stem cells: regulation of niche, self-renewal and differentiation, Arthritis Res. Ther., 2007, vol. 1, no. 204, pp..

  • Lai, R.C., Arslan, F., Tan, S.S., Tan, B., Choo, A., Lee, M.M., Chen, T.S., Teh, B.J., Eng, J.K., Sidik, H., Tanavde, V., Hwang, W.S., Lee, C.N., El Oakley, R.M., Pasterkamp, G., et al., Derivation and characterization of human fetal MSCs: an alternative cell source for large-scale production of cardioprotective microparticles, J. Mol. Cell. Cardiol., 2010a, vol. 48, no. 6, pp. 1215–1224.

    Article  CAS  PubMed  Google Scholar 

  • Lai, Y., Sun, Y., Skinner, C.M., Son, E.L., Lu, Z., Tuan, R.S., Jilka, R.L., Ling, J., and Chen, X.D., Reconstitution of marrow-derived extracellular matrix ex vivo: a robust culture system for expanding large-scale highly functional human mesenchymal stem cells, Stem Cells Dev., 2010b, vol. 19, no. 7, pp. 1095–1107.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lebedinskaya, O.V., Gorskaya, Yu.F., Shuklina, Ye.Yu., Latzinik, N.V., and Nesterenko, V.G., Age-related changes of number of stromal cells-precursors in marrow of animals, Morfologiya, 2004, vol. 126, no. 6, pp. 46–49.

    Google Scholar 

  • Lebedinskaya, O.V., Gorskaya, Yu.F., Shuklina, Ye.Yu., Latzinik, N.V., and Nesterenko, V.G., Analysis of the changes of stromal precursor cell numbers in the thymus and the spleen of animals of different age groups, Morfologiya, 2005, vol. 127, no. 3, pp. 41–44.

    Google Scholar 

  • Le Blanc, K., Immunomodulatory effects of fetal and adult mesenchymal stem cells, Cytotherapy, 2003, vol. 5, no. 6, pp. 485–489.

    Article  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, W.G. and Xu, X.X., The expression of N-cadherin, fibronectin during chondrogenic differentiation of MSC induced by TGF-beta (1), Chin. J. Traumatol., 2005, vol. 8, no. 6, pp. 349–351.

    PubMed  Google Scholar 

  • Lou, S., Gu, P., Chen, F., He, C., Wang, M., and Lu, C., The effect of bone marrow stromal cells on neuronal differentiation of mesencephalic neural stem cells in Spargue-Dawley rats, Brain Res., 2003, vol. 968, no. 1, pp. 114–121.

    Article  CAS  PubMed  Google Scholar 

  • Lund, A.W., Yener, B., Stegemann, J.P., and Plopper, G.E., The natural and engineered 3D microenvironment as a regulatory cue during stem cell fate determination, Tissue Eng., Part A, 2009, vol. 15, no. 3, pp. 371–380.

    Article  Google Scholar 

  • 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, no. 1, pp. 57–66.

    Article  CAS  PubMed  Google Scholar 

  • Mayanskaya, I.V., Goganova, A.Yu., Tolkacheva, N.I., Ashkinazi, V.I., and Mayanskii, A.N., Immune-suppressive effect of mesenchymal stem (stromal) cells, Immunologiya (Moscow), 2013, vol. 34, no. 2, pp. 122–128.

    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.

    Article  CAS  PubMed  Google Scholar 

  • Mendez-Ferrer, S., Michurina, T.V., Ferraro F., Mazloom, A.R., MacArthur, B.D., Lira, S.A., Scadden, D.T., Ma’ayan, A., Enikolopov, G.N., and Frenette, P.S., Mesenchymal and hematopoietic stem cells form a unique bone marrow niche, Nature, 2010, vol. 466, no. 7308, pp. 829–834.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mias, C., Lairez, O., Trouche, E., Roncalli, J., Calise, D., Seguelas, M.H., Ordener, C., Piercecchi-Marti, M.D., Auge, N., Salvayre, A.N., Bourin, P., Parini, A., and Cussac, D., Mesenchymal stem cells promote matrix metalloproteinase secretion by cardiac fibroblasts and reduce cardiac ventricular fibrosis after myocardial infarction, Stem Cells, 2009, vol. 27, no. 11, pp. 2734–2743.

    Article  CAS  PubMed  Google Scholar 

  • Mirmalek-Sani, S.-H., Tare, R.S., Morgan, S.M., Roach, H.I., Wilson, D.I., Hanley, N.A., and Oreffo, R.O.C., Characterization and multipotentiality of human fetal femur-derived cells: implications for skeletal tissue regeneration, Stem Cells, 2006, vol. 24, no. 4, pp. 1042–1053.

    Article  PubMed  Google Scholar 

  • Miura, Y., Gao, Z., Miura, M., Seo, B.M., Sonoyama, W., Chen, W., Gronthos, S., Zhang, L., and Shi, S., Mesenchymal stem cell-organized bone marrow elements: an alternative hematopoietic progenitor resource, Stem Cells, 2006, vol. 24, no. 11, pp. 2428–2436.

    Article  CAS  PubMed  Google Scholar 

  • Morigi, M., Imberti, B., Zoja, C., Corna, D., Tomasoni, S., Abbate, M., Rottoli, D., Angioletti, S., Benigni, A., Perico, N., Alison, M., and Remuzzi, G., Mesenchymal stem cells are renotropic, helping to repair the kidney and improve function in acute renal failure, J. Am. Soc. Nephrol., 2004, vol. 15, no. 7, pp. 1794–1804.

    Article  PubMed  Google Scholar 

  • Nicolaidou, V., Wong, M.M., Redpath, A.N., Ersek, A., Baban, D.F., Williams, L.M., Cope, A.P., and Horwood, N.J., Monocytes induce STAT3 activation in human mesenchymal stem cells to promote osteoblast formation, PLoS One, 2012, vol. 7, no. 7, p. e39871.

    Google Scholar 

  • Noiseux, N., Gnecchi, M., Lopez-Ilasaca, M., Zhang, L., Solomon, S.D., Deb, A., Dzau, V.J., and Pratt, R.E., Mesenchymal stem cells overexpressing Akt dramatically repair infarcted myocardium and improve cardiac function despite infrequent cellular fusion or differentiation, Mol. Ther., 2006, vol. 14, no. 6, pp. 840–850.

    Article  CAS  PubMed  Google Scholar 

  • Noth, U., Osyczka, A.M., Tuli, R., Hickok, N.J., Danielson, K.G., and Tuan, R.S., Multilineage mesenchymal differentiation potential of human trabecular bonederived cells, J. Orthop. Res., 2002, vol. 20, no. 5, pp. 1060–1069.

    Article  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 

  • Oshima, Y., Watanabe, N., Matsuda, K., Takai, S., Kawata, M., and Kubo, T., Behaviour of transplanted bone marrowderived GFP mesenchymal cells in osteochondral defect as a stimulation of autologous transplantation, J. Histochem. Cytochem., 2005, vol. 53, no. 2, pp. 207–216.

    Article  CAS  PubMed  Google Scholar 

  • Overstraeten-Schlögel van, N., Beguin, Y., and Gothot, A., Role of stromal-derived factor-1 in the hematopoieticsupporting activity of human mesenchymal stem cells, Eur. J. Haematol., 2006, vol. 76, no. 6, pp. 488–493.

    Article  CAS  Google Scholar 

  • Panepucci, R.A., Siufi, J.L., Silva, W.A., Jr, Proto-Siquiera, R., Neder, L., Orellana, M., Rocha, V., Covas, D.T., and Zago, M.A., Comparison of gene expression of umbilical cord vein and bone marrow-derived mesenchymal stem cells, Stem Cells, 2004, vol. 22, no. 7, pp. 1263–1278.

    Article  CAS  PubMed  Google Scholar 

  • Papaccio, G., Graziano, A., d’Aquino, R., Graziano, M.F., Pirozzi, G., Menditti, D., De Rosa, A., Carinci, F., and Laino, G., Long-term cryopreservation of dental pulp stem cells (SBP-DPSCs) and their differentiated osteoblasts: a cell source for tissue repair, J. Cell. Physiol., 2006, vol. 208, no. 2, pp. 319–325.

    Article  CAS  PubMed  Google Scholar 

  • Payushina, O.V., Domaratskaya, E.I., and Starostin, V.I., Cell composition and regulatory functions of stroma of embryonic liver, Tsitologiya, 2012, vol. 54, no. 5, pp. 369–380.

    Google Scholar 

  • Peng, L., Jia, Z., Yin, X., Zhang, X., Liu, Y., Chen, P., Ma, K., and Zhou, C., Comparative analysis of mesenchymal stem cells from bone marrow, cartilage, and adipose tissue, Stem Cells Dev., 2008, vol. 17, no. 4, pp. 761–773.

    Article  CAS  PubMed  Google Scholar 

  • Rafii, S., Mohle, R., Shapiro, F., Frey, B.M., and Moore, M.A., Regulation of hematopoiesis by microvascular endothelium, Leuk. Lymphoma, 1997, vol. 27, nos. 5-6, pp. 375–386.

    CAS  PubMed  Google Scholar 

  • Ramírez, M., Lucia, A., Gómez-Gallego, F., EsteveLanao, J., Pérez-Martínez, A., Foster, C., Andreu, A.L., Martin, M.A., Madero, L., Arenas, J., and GarcíaCastro, J., Mobilization of mesenchymal cells into blood in response to skeletal muscle injury, Br. J. Sports Med., 2006, vol. 40, no. 8, pp. 719–722.

    Article  PubMed Central  PubMed  Google Scholar 

  • Riekstina, U., Cakstina, I., Parfejevs, V., Hoogduijn, M., Jankovskis, G., Muiznieks, I., Muceniece, R., and Ancans, J., Embryonic stem cell marker expression pattern in human mesenchymal stem cells derived from bone marrow, adipose tissue, heart and dermis, Stem Cell Rev., 2009, vol. 5, no. 4, pp. 378–386.

    Article  CAS  PubMed  Google Scholar 

  • Rochefort, G.Y., Delorme, B., Lopez, A., Hérault, O., Bonnet, P., Charbord, P., Eder, V., and Domenech, J., Multipotential mesenchymal stem cells are mobilized into peripheral blood by hypoxia, Stem Cells, 2006, vol. 24, no. 10, pp. 2202–2208.

    Article  CAS  PubMed  Google Scholar 

  • Rojas, M., Xu, J., Woods, C.R., Mora, A.L., Spears, W., Roman, J., and Brigham, K.L., Bone marrow-derived mesenchymal stem cells in repair of the injured lung, Am. J. Respir. Cell. Mol. Biol., 2005, vol. 33, no. 2, pp. 145–152.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Roura, S., Farré, J., Soler-Botija, C., Llach, A., HoveMadsen, L., Cairó, J.J., Gódia, F., Cinca, J., and Bayer-Genis, A., Effect of aging on the pluripotential capacity of human CD105+ mesenchymal stem cells, Eur. J. Heart Failure, 2006, vol. 8, no. 6, pp. 555–563.

    Article  CAS  Google Scholar 

  • Rubtsov, Y.P., Suzdaltseva, Y.G., Goryunov, K.V., Kalinina, N.I., Sysoeva, V.Y., and Tkachuk, V.A., Regulation of immunity via multipotent mesenchymal stromal cells, Acta Nat. (Engl. Transl.), 2012, vol. 4, no. 1, pp. 23–31.

    CAS  Google Scholar 

  • Sági, B., Maraghechi, P., Urbán, V.S., Hegyi, B., Szigeti, A., Fajka-Boja, R., Kudlik, G., Német, K., Monostori, E., Gócza, E., and Uher, F., Positional identity of murine mesenchymal stem cells resident in different organs is determined in the postsegmentation mesoderm, Stem Cells Dev., 2012, vol. 21, no. 5, pp. 814–828.

    Article  PubMed  CAS  Google Scholar 

  • Salem, H.K. and Thiemermann, C., Mesenchymal stromal cells: current understanding and clinical status, Stem Cells, 2010, vol. 28, no. 3, pp. 585–596.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sasaki, M., Abe, R., Fujita, Y., Ando, S., Inokuma, D., and Shimizu, H., Mesenchymal stem cells are recruited into wounded skin and contribute to wound repair by trans-differentiation into multiple skin cell type, J. Immunol., 2008, vol. 180, no. 4, pp. 2581–2587.

    Article  CAS  PubMed  Google Scholar 

  • Sato, Y., Araki, H., Kato, J., Nakamura, K., Kawano, Y., Kobune, M., Sato, T., Miyanishi, K., Takayama, T., Takahashi, M., Takimoto, R., Iyama, S., Matsunaga, T., Ohtani, S., Matsuura, A., et al., Human mesenchymal stem cells xenografted directly to rat liver differentiated into human hepatocytes without fusion, Blood, 2005, vol. 106, no. 2, pp. 756–763.

    Article  CAS  PubMed  Google Scholar 

  • Schenk, S., Mal, N., Finan, A., Zhang, M., Kiedrowski, M., Popovic, Z., McCarthy, P.M., and Penn, M.S., Monocyte chemotactic protein-3 is a myocardial mesenchymal stem cell homing factor, Stem Cells, 2007, vol. 25, no. 1, pp. 245–251.

    Article  CAS  PubMed  Google Scholar 

  • Schofield, R., The relationship between the spleen colonyforming cell and the haemopoietic stem cell, Blood Cells, 1978, vol. 4, nos. 1-2, pp. 7–25.

    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.

    Article  CAS  PubMed  Google Scholar 

  • Shin, C.S., Lecanda, F., Sheikh, S., Weitzmann, L., Cheng, S.L., and Civitelli, R., Relative abundance of different cadherins defines differentiation of mesenchymal precursors into osteogenic, myogenic, or adipogenic pathways, J. Cell. Biochem., 2000, vol. 78, no. 4, pp. 566–577.

    Article  CAS  PubMed  Google Scholar 

  • Signore, M., Cerio, A.M., Boe, A., Pagliuca, A., Zaottini, V., Schiavoni, I., Fedele, G., Petti, S., Navarra, S., Ausiello, C.M., Pelosi, E., Fatica, A., Sorrentino, A., and Valtieri, M., Identity and ranking of colonic mesenchymal stromal cells, J. Cell. Physiol., 2012, vol. 227, no. 9, pp. 3291–3300.

    Article  CAS  PubMed  Google Scholar 

  • Srikanth, G.V.N., Tripathy, N.K., and Nityanand, S., Fetal cardiac mesenchymal stem cells express embryonal markers and exhibit differentiation into cells of all three germ layers, World J. Stem Cells, 2013, vol. 5, no. 1, pp. 26–33.

    Article  PubMed Central  PubMed  Google Scholar 

  • Stenderup, K., Justesen, J., Clausen, C., and Kassem, M., Aging is associated with decreased maximal life span and accelerate senescence of bone marrow stromal cells, Bone, 2003, vol. 33, no. 6, pp. 919–926.

    Article  PubMed  Google Scholar 

  • Sugiyama, D., Inoue-Yokoo, T., Fraser, S.T., Kulkeaw, K., Mizuochi, C., and Horio, Y., Embryonic regulation of the mouse hematopoietic niche, Sci. World J., 2011, vol. 11, pp. 1770–1780.

    Article  CAS  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Takashima, Y., Era, T., Nakao, K., Kondo, S., Kasuga, M., Smith, A.G., and Nishikawa, S., Neuroepithelial cells supply an initial transient wave of MSC differentiation, Cell, 2007, vol. 129, no. 7, pp. 1377–1388.

    Article  CAS  PubMed  Google Scholar 

  • Tan, Q., Liu, P.P., Rui, Y.F., and Wong, Y.M., Comparison of potentials of stem cells isolated from tendon and bone marrow for musculoskeletal tissue engineering, ssue Eng., Part A, 2012, vol. 18, nos. 7-8, pp. 840–851.

    Article  CAS  Google Scholar 

  • Tatarinova, O.S., Osipova, E.Yu., and Rymyantsev, S.A., Biological properties and possible clinical use of mesenchymal stem cells, Onkogematologiya, 2009, no. 4, pp. 33–44.

    Google Scholar 

  • Teo, G.S., Ankrum, J.A., Martinelli, R., Boetto, S.E., Simms, K., Sciuto, T.E., Dvorak, A.M., Karp, J.M., and Carman, C.V., Mesenchymal stem cells transmigrate between and directly through tumor necrosis factor-a-activated endothelial cells via both leukocytelike and novel mechanisms, Stem Cells, 2012, vol. 30, no. 11, pp. 2472–2486.

    Article  PubMed Central  CAS  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 

  • Ueno, T., Nakashima, A., Doi, S., Kawamoto, T., Honda, K., Yokoyama, Y., Doi, T., Higashi, Y., Yorioka, N., Kato, Y., Kohno, N., and Masaki, T., Mesenchymal stem cells ameliorate experimental peritoneal fibrosis by suppreßsing inflammation and inhibiting TGF-ß1 signaling, Kidney Int., 2013, vol. 84, no. 2, pp. 297–307.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vlodavsky I., Bar-Shavit, R., Ishai-Michaeli, R., Bashkin, P., and Fuks, Z., Extracellular sequestration and release of fibroblast growth factor: a regulatory mechanism? Trends Biochem. Sci., 1991, vol. 16, no. 7, pp. 268–271.

    Article  CAS  PubMed  Google Scholar 

  • Wagner, W., Roderburg, C., Wein, F., Diehlmann, A., Frankhauser, M., Schubert, R., Eckstein, V., and Ho, A.D., 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.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wang, H.S., Hung, S.C., Peng, S.T., Huang, C.C., Wei, H.M., Guo, Y.J., Fu, Y.S., Lai, M.C., and Chen, C.C., Mesenchymal stem cells in the Wharton’s jelly of the human umbilical cord, Stem Cells, 2004, vol. 22, no. 7, pp. 1330–1337.

    Article  PubMed  Google Scholar 

  • Wang, X.Y., Lan, Y., He, W.Y., Zhang, L., Yao, H.Y., Hou, C.M., Tong, Y., Liu, Y.L., Yang, G., Liu, X.D., Yang, X., Liu, B., and Mao, N., Identification of mesenchymal stem cells in aorta-gonad-mesonephros and yolk sac of human embryos, Blood, 2008, vol. 111, no. 4, pp. 2436–2443.

    Article  CAS  PubMed  Google Scholar 

  • Wang, X.Y., Liu, B., Yuan, C.H., Yao, H.Y., and Mao, N., Effect of bone marrow mesenchymal stem cells on hematopoietic differentiation of murine embryonic stem cells, Chin. J. Exp. Hematol., 2003, vol. 11, no. 4, pp. 329–334.

    Google Scholar 

  • Wenceslau, C.V., Miglino, M.A., Martins, D.S., Ambrósio, C.E., Lizier, N.F., Pignatari, G.C., and Kerkis, I., Mesenchymal progenitor cells from canine fetal tissues: yolk sac, liver, and bone marrow, Tissue Eng., Part A, 2011, vol. 17, nos. 17-18, pp. 2165–2176.

    Article  CAS  Google Scholar 

  • 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, no. 2, pp. 142–146.

    CAS  PubMed  Google Scholar 

  • Yang, M.C., Chi, N.H., Chou, N.K., Huang, Y.Y., Chung, T.W., Chang, Y.L., Liu, H.C., Shieh, M.J., and Wang, S.S., The influence of rat mesenchymal stem cell CD44 surface markers on cell growth, fibronectin expression, and cardiomyogenic differentiation on silk fibroin—hyaluronic acid cardiac patches, Biomaterials, 2010, vol. 31, no. 5, pp. 854–862.

    Article  CAS  PubMed  Google Scholar 

  • Yoon, Y.S., Wecker, A., Heyd, L., Park, J.S., Tkebuchava, T., Kusano, K., Hanley, A., Scadova, H., Qin, G., Cha, D.H., Johnson, K.L., Aikawa, R., Asahara, T., and Losordo, D.W., Clonally expanded novel multipotent stem cells from human bone marrow regenerate myocardium after myocardial infarction, J. Clin. Invest., 2005, vol. 115, no. 2, pp. 326–338.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yoshimura, H., Muneta, T., Nimura, A., Yokoyama, A., Koga, H., and Sekiya, I., Comparison of rat mesenchymal stem cells derived from bone marrow, synovium, periosteum, adipose tissue, and muscle, Cell Tissue Res., 2007, vol. 327, no. 3, pp. 449–462.

    Article  CAS  PubMed  Google Scholar 

  • Zemel’ko, V.I., Grinchuk, T.M., Domnina, A.P., Artzibasheva, I.V., Zenin, V.V., Kirsanov, A.A., Bichevaya, N.K., Korsak, V.S., and Nikolsky, N.N., Multipotent mesenchymal stem cells of desquamated endometrium: isolation, characterization and use as feeder layer for maintenance of human embryonic stem cell lines, Tsitologiya, 2011, vol. 53, no. 12, pp. 919–929.

    Google Scholar 

  • Zhang, J., An, Y., Gao, L.N., Zhang, Y.J., Jin, Y., and Chen, F.M., The effect of aging on the pluripotential capacity and regenerative potential of human periodontal ligament stem cells, Biomaterials, 2012, vol. 33, no. 29, pp. 6974–6986.

    Article  CAS  PubMed  Google Scholar 

  • Zhuang, Y., Chen, X., Xu, M., Zhang, L.Y., and Xiang, F., Chemokine stromal cell-derived factor 1/CXCL12 increases homing of mesenchymal stem cells to injured myocardium and neovascularization following myocardial infarction, Chin. Med. J., 2009, vol. 122, no. 2, pp. 183–187.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

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

    O. V. Payushina

Authors
  1. O. V. Payushina
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to O. V. Payushina.

Additional information

Original Russian Text © O.V. Payushina, 2015, published in Zhurnal Obshchei Biologii, 2015, Vol. 76, No. 2, pp. 161–172.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Payushina, O.V. Localization and functions of mesenchymal stromal cells in vivo. Biol Bull Rev 6, 1–10 (2016). https://doi.org/10.1134/S2079086416010059

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S2079086416010059

Keywords

Search

Navigation