C-Myc Proto-Oncogene Expression During Newt Limb Regeneration

  • Jacqueline Géraudie
  • Jacques Hourdry
  • Keith Boehm
  • Marcus Singer
  • Marcel Mechali
Part of the NATO ASI Series book series (NSSA, volume 172)


Utilizing the method of in situ hybridization, myc-homologous RNA transcripts were detected in histological sections of the newt limb regenerate. A radiolabeled Xenopus myc-cDNA was used as probe. Autoradiographic grains representing myc-homologous RNAs were observed in cells of the thickened wound epidermis, irrespective of the layer examined. Further, mesenchymatous-like cells which form the blastema also contained multiple grains, indicating that these cells possess myc-like RNA molecules. The presence of RNAs, homologous to the myc proto-oncogene in cells of the regenerating newt limb indicate that a myc-related gene is expressed in these cells during the regenerative process and, therefore, may play an important regulatory role, as myc gene expression has been implicated in the control of cellular proliferation in other systems. Our results are discussed against the background of literature on c-myc proto-oncogene expression.


Limb Regeneration Blastemal Cell Wound Epidermis Notophthalmus Viridescens Actively Cycling Cell 
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  1. Barger, P.M. and Tassava, R.A., 1985, Kinetics of cell cycle entry in innervated and denervated forelimb stumps of larval Ambystoma, J.Exp.Zool., 233:151–154.CrossRefGoogle Scholar
  2. Bentley-Lawrence, J. and Singer, R.H., 1985, Quantitative analysis of in situ hybridization methods for the detection of actin gene expression, Nucleic Acids Res., 13:1777–1799.CrossRefGoogle Scholar
  3. Biesiada, E. and Chorazy 1988, Expression of “cell-cycle-dependent” genes in regenerating rat liver, Cell Biol. Int. Rep., 12:483–492.PubMedCrossRefGoogle Scholar
  4. Bishop, J.M., 1985, Trends in oncogenes, TIGS., 1:245–249.CrossRefGoogle Scholar
  5. Boilly, B., Oudkhir, M. and Lassalle, B., 1985, Control of the blastemal cell cycle by peripheral nervous system during newt limb regeneration; continuous labelling analysis, Biol. Cell., 55:107–112.PubMedCrossRefGoogle Scholar
  6. Brahic, C. and Haase, A.T., 1978, Detection of viral sequences of low reiteration frequency by in situ hybridization, Proc. Natl. Acad. Sci. USA., 75:6125–6129.PubMedCrossRefGoogle Scholar
  7. Cole, M.D., 1986, The myc oncogene: its role in transformation and differentiation, Ann. Rev. Genet., 20:361–384.PubMedCrossRefGoogle Scholar
  8. Goldhamer, D.J. and Tassava, R.A., 1987, An analysis of proliferative activity in innervated and denervated forelimb regenerates of the newt, Notophthalmus viridescens. Development, 100:619–628.Google Scholar
  9. Goyette, M., Petropoulos, C.J., Shank, P.R. and Fausto, N., 1984, Regulated transcription of c-ki-ras and c-myc during compensatory growth of rat liver, Mol. Cell. Biol., 4:1493–1498.PubMedGoogle Scholar
  10. Harm, S.R., Thompson, C.B. and Eisenman, R.N., 1985, c-myc oncogene protein synthesis is independent of the cell cycle in human and avian cells, Nature, 314:366–369.CrossRefGoogle Scholar
  11. Hay, E.D. and Fischman, D.A., 1961, Origin of the blastema in regenerating limb of the newt Triturus viridescens. An autoradiographic study using tritiated thymidine to follow cell proliferation and migration, Dev. Biol., 3:20–59.CrossRefGoogle Scholar
  12. Heldin, CH., and Westermark, B., 1984, Growth factors: mechanism of action and relation to oncogenes, Cell, 37:9–20.PubMedCrossRefGoogle Scholar
  13. Hoffman, C.W. and Dent, J.N., 1977, Hormonal effects on mitotic rhythm in the epidermis of the red-spotted newt, Gen. Comp. Endocrinol., 32:512–521.PubMedCrossRefGoogle Scholar
  14. Hourdry, J., Brulfert, A., Gusse, M., Schoevaert, D., Taylor, M. and Mechali, M., Localization of c-myc expression during oogenesis and embryonic development in Xenopus laevis, Development (in press).Google Scholar
  15. Hourdry, J., Géraudie, J., Singer, M. and Mechali, M., 1988, Expression of the c-myc proto-oncogene in the forelimb regenerate of the newt Notophthalmus viridescens, visualized by in situ hybridization. in: “Regeneration and Development”, S. Inoue, ed., Okada Printing and Publishing Company, Maebashi, Japan.Google Scholar
  16. Kaczmarek, L., 1986, Proto-oncogene expression during the cell cycle, Lab. Invest., 543:365–376.Google Scholar
  17. Kelly, K., Cochran, B.H., Stiles, C.D. and Leder, P., 1983, Cell-specific regulation of the c-myc gene by lymphocyte mitogens and platelet-derived growth factor, Cell, 35:603–610.PubMedCrossRefGoogle Scholar
  18. King, M.W., Roberto, J.M. and Eisenman, R.A., 1986, Expression of the c-myc proto-oncogene during development of Xenopus laevis, Mol. Cell. Biol., 6:4499–4508.PubMedGoogle Scholar
  19. Lombard-Des Gouttes, M.N., 1988, Rat liver regeneration and plasma factors: an overview of some early events in the compensatory growth process. in: “Regeneration and Development”, S. Inoue Ed., Okada Printing and Publishing Company, Maebashi, Japan.Google Scholar
  20. Maden, M., 1978, Neurotrophic control of the cell cycle during amphibian limb regeneration, J. Embryo1. Exp. Morph., 48:169–175.Google Scholar
  21. Makino, R., Hasaki, K. and Sugimura, T., 1984, c-myc transcript is induced in rat liver at a very early stage of regeneration by cycloheximide treatment, Nature. 310:697–698.PubMedCrossRefGoogle Scholar
  22. Muller, R., 1986, Proto-oncogenes and differentiation, TIBS, 11:129–132.Google Scholar
  23. Olsen, C.L. and Tassava, R.A., 1984, Cell cycle and histological effects of reinnervation in denervated forelimb stumps of larval Ambystoma, J. Exp. Zool., 229:247–258.PubMedCrossRefGoogle Scholar
  24. O’Steen, W.K. and Walker, B.E., 1961, Radioautographic studies of regeneration in the common newt: II. Regeneration of the forelimb, Anat. Rec., 139:547–555.CrossRefGoogle Scholar
  25. Petavy, G., 1985, Reliable preparative procedures for the cytological study of yolk-laden insect eggs and embryos, Stain Tech., 60:321–330.Google Scholar
  26. Pfeiffer-Ohlsson, S., Goustin, A.S., Rydnert, J., Wahlstrom, T., Bjersing, L., Stehelin, D. and Ohlsson, R., 1984, Spatial and temporal pattern of cellular myc oncogene expression in developing human placenta: implications for embryonic cell proliferation, Cell, 38:585–596.CrossRefGoogle Scholar
  27. Riddiford, L.M., 1960, Autoradiographic studies of tritiated thymidine infused into the blastema of the early regenerate in the adult newt Triturus, J. Exp. Zool., 144:25–31.PubMedCrossRefGoogle Scholar
  28. Schmidt, A.J., 1968, “Cellular biology of vertebrate regeneration and repair”, The University of Chicago Press, Chicago and London.Google Scholar
  29. Sicard, R.E., 1985, “Regulation of vertebrate limb regeneration”, R.E. Sicard, ed., Oxford University Press, New York, Oxford.Google Scholar
  30. Singer, M., 1952, The influence of the nerve in regeneration of the amphibian extremity, Quart. Rev. Biol., 27:169–200.PubMedCrossRefGoogle Scholar
  31. Singer, M., 1978, On the nature of the neurotrophic phenomenon in urodele limb regeneration, Am. Zool., 18:829–841.Google Scholar
  32. Taylor, M.V., Gusse, M., Evan, G.I., Dathan, N. and Mechali, M., 1986, Xenopus c-myc protooncogene during development: Expression as a stable maternal mRNA uncoupled from cell division, EMBO J., 5:3563–3570.PubMedGoogle Scholar
  33. Thompson, C.B., Challoner, P.B., Neiman, P.E. and Groudine, M., 1985, Levels of c-myc oncogene mRNA are invariant throughout the cell cycle, Nature, 314:363–366.PubMedCrossRefGoogle Scholar
  34. Thompson, N.L., Mead, J.E., Braun, L., Goyette, M., Shank, P.R. and Fausto, N., 1986, Sequential protooncogene expression during rat liver regeneration, Cancer Research, 46:3111–3117.PubMedGoogle Scholar
  35. Tomlinson, B.L., Goldhamer, D.J., Barger, P.M. and Tassava, R.A., 1985, Punctuated cell cycling in the regeneration blastema of urodele amphibians: A hypothesis, Differentiation, 28:195–199.CrossRefGoogle Scholar
  36. Varmus, H.E., 1984, The molecular genetics of cellular oncogenes, Ann. Rev. Genet., 8:553–612.CrossRefGoogle Scholar
  37. Wallace, H., 1981, “Vertebrate limb regeneration”, John Wiley and Sons, New York.Google Scholar
  38. Zimmerman, K.A., Yancopoulos, G.D., Collum, R.G., Smith, R.K., Kohl, N.E., 1986, Differential expression of myc family genes during murine development, Nature 319:783–790.CrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1989

Authors and Affiliations

  • Jacqueline Géraudie
    • 1
  • Jacques Hourdry
    • 2
  • Keith Boehm
    • 3
  • Marcus Singer
    • 3
  • Marcel Mechali
    • 2
  1. 1.Laboratoire d’Anatomie CompareeUniversité Paris VIIParis Cedex 05France
  2. 2.Institut Jacques MonodParis Cedex 05France
  3. 3.Department of Anatomy, School of MedicineCase Western Reserve UniversityClevelandUSA

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