International Journal of Hematology

, Volume 79, Issue 5, pp 488–494 | Cite as

Hematopoietic Progenitor Cells Residing in Muscle Engraft into Bone Marrow following Transplantation

  • Kathrin Terres Bauermeister
  • Stephanie Stölting
  • Piotr M. Kaczmarek
  • Roger Nadrowitz
  • Thomas Wagner
  • Stefan O. Peters


Hematopoietic and mesenchymal stem cells can potentially be the same cell type or adhere simultaneously in both bone marrow (BM) and muscle. In this study, we asked whether murine BM-derived cells could be tracked in muscle tissue after BM transplantation and whether muscle-derived cells have hematopoietic potential. To answer the first question, we transplanted BM from male BALB/c mice into irradiated female recipients and analyzed for engraftment. We used quantitative polymerase chain reaction (PCR) and fluorescent in situ hybridization techniques for Y chromosome—specific gene probes. A high number of BM-derived cells were located in both the intravascular and extravascular spaces in muscle tissue after BM transplantation. To answer the second question, we analyzed colony-forming potential in vitro with soft-agar assays and the competitive engraftment potential in vivo of muscle-derived cells. Engraftment levels of male cell populations were tested by quantitative PCR. The long-term engraftment potential of muscle-derived cells was low compared with that of BM. We conclude that there is intensive cellular trafficking between BM and muscle tissue. The engraftment potential of muscle-derived stem cells into BM is low and corresponds to the low amounts of hematopoietic colony-forming cells found in muscle tissue.

Key words

Hematopoietic stem cells Muscle-derived stem cells Competitive bone marrow transplantation BALB/c 


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  1. 1.
    Bittner RE, Schofer C, Weipoltshammer K, et al. Recruitment of bone-marrow-derived cells by skeletal and cardiac muscle in adult dystrophic mdx mice. Anat Embryol (Berl). 1999;199:391–396.CrossRefGoogle Scholar
  2. 2.
    Brazelton TR, Rossi FM, Keshet GI, Blau HM. From marrow to brain: expression of neuronal phenotypes in adult mice. Science. 2000;290:1775–1779.CrossRefGoogle Scholar
  3. 3.
    Gussoni E, Soneoka Y, Strickland CD, et al. Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature. 1999;401:390–394.Google Scholar
  4. 4.
    Jackson KA, Mi T, Goodell MA. Hematopoietic potential of stem cells isolated from murine skeletal muscle. Proc Natl Acad Sci U S A. 1999;96:14482–14486.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Krause DS, Theise ND, Collector MI, et al. Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell. 2001;105:369–377.CrossRefGoogle Scholar
  6. 6.
    Lagasse E, Connors H, Al Dhalimy M, et al. Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat Med. 2000;6:1229–1234.CrossRefGoogle Scholar
  7. 7.
    Mezey E, Chandross KJ, Harta G, Maki RA, McKercher SR. Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow. Science. 2000;290:1779–1782.CrossRefGoogle Scholar
  8. 8.
    Goodell MA, Jackson KA, Majka SM, et al. Stem cell plasticity in muscle and bone marrow. Ann N Y Acad Sci. 2001;938:208–218.CrossRefGoogle Scholar
  9. 9.
    Butcher EC. Leukocyte-endothelial cell recognition: three (or more) steps to specificity and diversity. Cell. 1991;67:1033–1036.CrossRefPubMedGoogle Scholar
  10. 10.
    Ferrari G, Cusella-De Angelis G, Coletta M, et al. Muscle regeneration by bone marrow-derived myogenic progenitors. Science. 1998;279:1528–1530.CrossRefGoogle Scholar
  11. 11.
    Peters SO, Bauermeister K, Simon JP, Branke B, Wagner T. Quantitative polymerase chain reaction-based assay with fluorogenic Y-chromosome specific probes to measure bone marrow chimerism in mice. J Immunol Methods. 2002;260:109–116.CrossRefPubMedGoogle Scholar
  12. 12.
    Schutte B, Reynders MM, Bosman FT, Blijham GH. Studies with anti-bromodeoxyuridine antibodies, II: simultaneous immunocyto-chemical detection of antigen expression and DNA synthesis by in vivo labeling of mouse intestinal mucosa. J Histochem Cytochem. 1987;35:371–374.CrossRefPubMedGoogle Scholar
  13. 13.
    Speel EJ, Kamps M, Bonnet J, Ramaekers FC, Hopman AH. Multicolour preparations for in situ hybridization using precipitating enzyme cytochemistry in combination with reflection contrast microscopy. Histochemistry. 1993;100:357–366.CrossRefPubMedGoogle Scholar
  14. 14.
    Balazs M, Mayall BH, Waldman FM. Simultaneous analysis of chromosomal aneusomy and 5-bromodeoxyuridine incorporation in MCF-7 breast tumor cell line. Cancer Genet Cytogenet. 1991;57:93–102.CrossRefPubMedGoogle Scholar
  15. 15.
    Speel EJ, Herbergs J, Ramaekers FC, Hopman AH. Combined immunocytochemistry and fluorescence in situ hybridization for simultaneous tricolor detection of cell cycle, genomic, and phenotypic parameters of tumor cells. J Histochem Cytochem. 1994;42:961–966.CrossRefPubMedGoogle Scholar
  16. 16.
    Kawada H, Ogawa M. Bone marrow origin of hematopoietic progenitors and stem cells in murine muscle. Blood. 2001;98:2008–2013.CrossRefPubMedGoogle Scholar
  17. 17.
    Farace F, Guillier M, Vainchenker W, Turhan AG. Lethally irradiated mice transplanted with muscle-derived stem cells have chimeric hematopoiesis [abstract]. Blood. 2000;96:275a.Google Scholar
  18. 18.
    McKinney-Freeman SL, Jackson KA, Camargo FD, Ferrari G, Mavilio F, Goodell MA. Muscle-derived hematopoietic stem cells are hematopoietic in origin. Proc Natl Acad Sci USA. 2002;99:1341–1346.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Issarachai S, Priestley GV, Nakamoto B, Papayannopoulou T. Cells with hemopoietic potential residing in muscle are itinerant bone marrow-derived cells. Exp Hematol. 2002;30:366–373.CrossRefPubMedGoogle Scholar

Copyright information

© The Japanese Society of Hematology 2004

Authors and Affiliations

  • Kathrin Terres Bauermeister
    • 1
  • Stephanie Stölting
    • 1
  • Piotr M. Kaczmarek
    • 2
  • Roger Nadrowitz
    • 3
  • Thomas Wagner
    • 1
  • Stefan O. Peters
    • 1
  1. 1.Division of HematologyMedical Department I, Medical University of LuebeckLuebeckGermany
  2. 2.Division of CardiologyMedical Department IILuebeckGermany
  3. 3.Radiation OncologyMedical University of LuebeckLuebeckGermany

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