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Pluripotent mesenchymal stem cells reside within avian connective tissue matrices

  • Growth, Differentiation, And Senescence
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Summary

Recent studies have noted the presence of putative stem cells derived from the connective tissues associated with skeletal muscle, heart, and dermis. Long-term continuous cultures of these cells from each tissue demonstrated five distinct phenotypes of mesodermal origin, i.e. muscle, fat, cartilage, bone, and connective tissue. Clonal analysis was performed to determine whether these morphologies were the result of a mixed population of lineage-committed stem cells or the differentiation of pluripotent stem cells or both. Putative stem cells from four tissues (skeletal muscle, dermis, atria, and ventricle) were isolated and cloned. Combined, 1158 clones were generated from the initial cloning and two subsequent subclonings. Plating efficiency approximated 5.8%. Approximately 70% of the 1158 clones displayed a pure stellate morphology, while the remaining clones contained a mixture of stellate, chondrogenic- or osteogenic-like morphologies or both. When cultured in the presence of dexamethasone, cells from all clones differentiated in a time- and concentration-dependent manner into muscle, fat, cartilage, and bone. These results suggest that pluripotent mesenchymal stem cells are present within the connective tissues of skeletal muscle, dermis, and heart and may prove useful for studies concerning the regulation of stem cell differentiation, wound healing, and tissue restoration, replacement and repair.

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References

  • Armand, O.; Boutineau, A.-M.; Mauger, A., et al. Origin of satellite cells in avian skeletal muscles. Arch. Anat. Microsc. Morphol. 72:163–181; 1983.

    CAS  Google Scholar 

  • Bader, D.; Masaki, T.; Fischman, D. A. Immunochemical analysis of myosin heavy chain during avian myogenesis in vivo and in vitro. J. Cell Biol. 95:763–770; 1982.

    Article  PubMed  CAS  Google Scholar 

  • Bischoff, R. Enzymatic liberation of myogenic cells from adult rat muscle. Anat. Rec. 180:645–662; 1974.

    Article  PubMed  CAS  Google Scholar 

  • Bischoff, R. Tissue culture studies on the origin of myogenic cells during muscle regeneration in the rat. In: Mauro, A.; Bischoff, R.; Carlson, B. M., et al., eds. Muscle regeneration. New York: Raven Press; 1979:13–29.

    Google Scholar 

  • Bischoff, R. Proliferation of muscle satellite cells on intact myofibers in culture. Dev. Biol. 115:129–139; 1986a.

    Article  PubMed  CAS  Google Scholar 

  • Bischoff, R. A satellite cell mitogen from crushed adult muscle. Dev. Biol. 115:140–147; 1986b.

    Article  PubMed  CAS  Google Scholar 

  • Caplan, A. I. A simplified procedure for preparing myogenic cells for culture. J. Embryol. Exp. Morphol. 36:175–181; 1976.

    PubMed  CAS  Google Scholar 

  • Caplan, A. I. Mesenchymal stem cells. J. Orthop. Res. 9:641–650; 1991.

    Article  PubMed  CAS  Google Scholar 

  • Carlson, B. M. The regeneration of skeletal muscle—a review. Am. J. Anat. 137:119–150; 1973.

    Article  PubMed  CAS  Google Scholar 

  • Carlson, B. M. Relationship between tissue and epimorphic regeneration of skeletal muscle. In: Mauro, A.; Bischoff, R.; Carlson, B. M., et al., eds. Muscle regeneration. New York: Raven Press; 1979:57–71.

    Google Scholar 

  • Carlson, B. M. Regeneration of entire skeletal muscles. Fed. Proc. 45:1456–1460; 1986.

    PubMed  CAS  Google Scholar 

  • Carlson, B. M.; Faulkner, J. A. The regeneration of skeletal muscle fibers following injury. Med. Sci. Sports Exercise 15:187–198; 1983.

    Article  CAS  Google Scholar 

  • Florini, J. R.; Magri, K. A. Effects of growth factors on myogenic differentiation. Am. J. Physiol. 256(25):C701-C711; 1989.

    PubMed  CAS  Google Scholar 

  • Grigoriadis, A. E.; Heersche, J. N. M.; Aubin, J. E. Differentiation of muscle, fat, cartilage, and bone from progenitor cells present in a bonederived clonal cell population: effect of dexamethasone. J. Cell Biol. 106:2139–2151; 1988.

    Article  PubMed  CAS  Google Scholar 

  • Humason, G. Animal tissue techniques, 3rd ed. San Francisco: W. H. Freeman and Co.; 1972.

    Google Scholar 

  • Levander, G. Induction phenomena in tissue regeneration. Baltimore: Williams & Wilkins; 1964.

    Google Scholar 

  • Lucas, P. A.; Syftestad, G. T.; Caplan, A. I. A water-soluble fraction from adult bone stimulates the differentiation of cartilage in explants of embryonic muscle. Differentiation 37:47–52; 1988.

    Article  PubMed  CAS  Google Scholar 

  • Mancini, M. L.; Wright, R. P.; Lucas, P. A., et al. Isolation of putative mesenchymal stem cells from embryonic chick heart. In Vitro Cell. Dev. Biol. 28:154A; 1992.

  • Mauro, A. Satellite cell of skeletal muscle fibers. J. Biophys. Biochem. Cytol. 9:493–495; 1961.

    Article  PubMed  CAS  Google Scholar 

  • Mauro, A.; Shafiq, S. A.; Milhorat, A. T. Regeneration of striated muscle, and myogenesis. Amsterdam: Excerpta Medica; 1970.

    Google Scholar 

  • Mauro, A.; Bischoff, R.; Carlson, B. M., et al. Muscle regeneration. New York: Raven Press; 1979.

    Google Scholar 

  • Moss, F. P.; Leblond, C. P. Satellite cells as the source of nuclei in muscles of growing rats. Anat. Rec. 170:421–436; 1971.

    Article  PubMed  CAS  Google Scholar 

  • Nakahara, H.; Bruder, S. P.; Goldberg, V. M., et al. In vivo osteochondrogenic potential of cultured cells derived from the periosteum. Clin. Orthop. Rel. Res. 259:223–232; 1990.

    Google Scholar 

  • Nathanson, M. A.; Hilfer, S. R.; Searles, R. L. Formation of cartilage by non-chondrogenic cell types. Dev. Biol. 64:99–117; 1978.

    Article  PubMed  CAS  Google Scholar 

  • Nathanson, M. A.; Hay, E. D. Analysis of cartilage differentiation from skeletal muscle grown in bone matrix. I. Ultrastructural aspects. Dev. Biol. 78:301–331; 1980.

    Article  PubMed  CAS  Google Scholar 

  • Ohgushi, H.; Goldberg, V. M.; Caplan, A. I. Heterotopic osteogenesis in porous ceramics induced by bone marrow cells. J. Orthop. Res. 7:568–578; 1989a.

    Article  PubMed  CAS  Google Scholar 

  • Ohgushi, H.; Goldberg, V. M.; Caplan, A. I. Repair of segmental long bone defect by composite graft of marrow cells and porous calcium phosphate ceramic. Acta Orthop. Scand. 60:334–339; 1989b.

    Article  PubMed  CAS  Google Scholar 

  • Polezhaev, L. V. Regeneration by induction (In Russian). Moscow: Izdatel Meditsina; 1977.

    Google Scholar 

  • Schultz, E. A quantitative study of satellite cells in regenerated soleus and extensor digitorum longus muscles. Anat. Rec. 208:501–506; 1984.

    Article  PubMed  CAS  Google Scholar 

  • Schultz, E.; Jaryszak, D. L. Effects of skeletal muscle regeneration on the proliferation potential of satellite cells. Mech. Ageing Dev. 30:63–72; 1985.

    Article  PubMed  CAS  Google Scholar 

  • Schultz, E.; Jaryszak, D. L.; Valliere, C. R. Response of satellite cells to focal skeletal muscle injury. Muscle Nerve 8:217–222; 1985.

    Article  PubMed  CAS  Google Scholar 

  • Snow, M. H. Myogenic cell formation in regenerating rat skeletal muscle injured by mincing. I. A fine structural study. Anat. Rec. 188:181–200; 1977a.

    Article  PubMed  CAS  Google Scholar 

  • Snow, M. H. Myogenic cell formation in regenerating rat skeletal muscle injured by mincing. II. An autoradiographic study. Anat. Rec. 188:201–218; 1977b.

    Article  PubMed  CAS  Google Scholar 

  • Snow, M. H. An autoradiographic study of satellite cell differentiation into regenerating myotubes following transplantation of muscle in young rats. Cell Tiss. Res. 186:535–540; 1978.

    Article  CAS  Google Scholar 

  • Snow, M. H. Origin of regenerating myoblasts in mammalian skeletal muscle. Muscle regeneration. In: Mauro, A., ed. New York: Raven Press; 1979:91–100.

    Google Scholar 

  • Stockdale, F. E.; Holtzer, H. DNA synthesis and myogenesis. Exp. Cell Res. 24:508–520; 1961.

    Article  PubMed  CAS  Google Scholar 

  • Urist, M. R.; Hay, P. H.; Dubuc, F., et al. Osteogenic competence. Clin. Orthop. 64:194–220; 1969.

    PubMed  CAS  Google Scholar 

  • Wright, R. P.; Mancini, M. L.; Lucas, P. A., et al. Isolation of putative mesenchymal stem cells from embryonic chick skin. In Vitro Cell. Dev. Biol. 28:156A; 1992.

  • Young, H. E.; Bailey, C. F.; Dalley, B. K., et al. Histological analysis of limb regeneration in post metamorphic adultAmbystoma. Anat. Rec. 212:183–194; 1985.

    Article  PubMed  CAS  Google Scholar 

  • Young, H. E.; Dalley, B. K.; Markwald, R. R. Glycoconjugates in normal wound tissue matrices during the initiation phase of limb regeneration in adultAmbystoma. Anat. Rec. 223:231–241; 1989a.

    Article  PubMed  CAS  Google Scholar 

  • Young, H. E.; Carrino, D. A.; Caplan, A. I. Histochemical analysis of newly synthesized and accumulated sulfated glycosaminglycans during musculogenesis in the embryonic chick leg. J. Morphol. 201:85–103; 1989b.

    Article  PubMed  CAS  Google Scholar 

  • Young, H. E.; Morrison, D. C.; Martin, J. D., et al. Cryopreservation of embryonic chick myogenic lineage-committed stem cells. J. Tissue Cult. Methods 13:275–284; 1991.

    Article  Google Scholar 

  • Young, H. E.; Ceballos, E. M.; Smith, J. C., et al. Isolation of embryonic chick myosatellite and pluripotent stem cells. J. Tissue Cult. Methods 14:85–92; 1992a.

    Article  Google Scholar 

  • Young, H. E.; Lucas, P. A. Isolation of putative mesenchymal stem cells from the skeletal muscle of embryonic chick and postnatal mouse. In Vitro Cell. Dev. Biol. 28:156A; 1992b.

  • Young, H. E.; Sippel, J.; Putnam, L. S., et al. Enzyme-linked immuno-culture assay. J. Tissue Cult. Methods 14:31–36; 1992c.

    Article  Google Scholar 

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Authors and Affiliations

  1. Division of Basic Medical Science, Mercer University School of Medicine, 1550 College Street, 31207, Macon, Georgia

    H. E. Young

  2. Department of Surgery, Mercer University School of Medicine, 1550 College Street, 31207, Macon, Georgia

    H. E. Young, J. C. Smith, M. L. Mancini, R. P. Wright, B. L. Ragan & Ian Bushell

  3. Department of Biology, Wesleyan College, 31297, Macon, Georgia

    E. M. Ceballos & J. C. Smith

  4. Department of Surgery, Mercer University School of Medicine at the Medical Center of Central Georgia, 31206, Macon, Georgia

    P. A. Lucas

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  1. H. E. Young
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  2. E. M. Ceballos
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  3. J. C. Smith
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  4. M. L. Mancini
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  5. R. P. Wright
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  6. B. L. Ragan
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  7. Ian Bushell
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  8. P. A. Lucas
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Young, H.E., Ceballos, E.M., Smith, J.C. et al. Pluripotent mesenchymal stem cells reside within avian connective tissue matrices. In Vitro Cell Dev Biol - Animal 29, 723–736 (1993). https://doi.org/10.1007/BF02631429

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  • DOI: https://doi.org/10.1007/BF02631429

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