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Published 13 May 2002. doi:10.1083/jcb.200108047
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© The Rockefeller University Press, 0021-9525/2002/5/693 $5.00
The Journal of Cell Biology, Volume 157, Number 4, May 13, 2002 693-702

Article

Myogenic cell proliferation and generation of a reversible tumorigenic phenotype are triggered by preirradiation of the recipient site



Jennifer E. Morgan1, Jacqueline G. Gross1, Charles N. Pagel1, Jonathan R. Beauchamp1, Ariberto Fassati2, Adrian J. Thrasher3, James P. Di Santo4, Ivan B. Fisher1,5,6, Xu Shiwen5, David J. Abraham5 and Terence A. Partridge1

1 Muscle Cell Biology Group, Medical Research Council Clinical Sciences Centre, Faculty of Medicine, Imperial College School of Technology and Medicine, London W12 0NN, UK
2 Wohl Virion Centre, Windeyer Institute, University College London Medical School, London W1T, UK
3 Molecular Immunology Unit, Institute of Child Health, London WC1N 1EH, UK
4 Unité des Cytokines et Développement Lymphoide, INSERM EMI-0101, Département d'Immunologie, Institut Pasteur, 75724 Paris, France
5 Department of Rheumatology, Division of Medicine, Royal Free and University College Medical School, London NW3 2PF, UK
6 Department of Paediatrics and Neonatal Medicine, Imperial College School of Technology and Medicine, London W12 ONN, UK

Address correspondence to Jennifer E. Morgan, Muscle Cell Biology Group, Medical Research Council Clinical Sciences Centre, Faculty of Medicine, Imperial College School of Technology and Medicine, Hammersmith Hospital Campus, Du Cane Road, London W12 ONN, UK. Tel.: 02-08-383-8262. Fax: 02-08-383-8264. E-mail: jmorgan{at}csc.mrc.ac.uk

Environmental influences have profound yet reversible effects on the behavior of resident cells. Earlier data have indicated that the amount of muscle formed from implanted myogenic cells is greatly augmented by prior irradiation (18 Gy) of the host mouse muscle. Here we confirm this phenomenon, showing that it varies between host mouse strains. However, it is unclear whether it is due to secretion of proliferative factors or reduction of antiproliferative agents. To investigate this further, we have exploited the observation that the immortal myogenic C2 C12 cell line forms tumors far more rapidly in irradiated than in nonirradiated host muscle. We show that the effect of preirradiation on tumor formation is persistent and dose dependent. However, C2 C12 cells are not irreversibly compelled to form undifferentiated tumor cells by the irradiated muscle environment and are still capable of forming large amounts of muscle when reimplanted into a nonirradiated muscle. In a clonal analysis of this effect, we discovered that C2 C12 cells have a bimodal propensity to form tumors; some clones form no tumors even after extensive periods in irradiated graft sites, whereas others rapidly form extensive tumors. This illustrates the subtle interplay between the phenotype of implanted cells and the factors in the muscle environment.

Key Words: radiation; neoplasia; skeletal muscle; cell transplantation; muscle precursor cell


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