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Expression of transcription factor c-Rel and apoptosis occurrence in polydactylous and syndactylous limb buds of the talpid3 mutant chick embryo

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Abstract

The chicken proto-oncogene c-rel encodes a transcription factor of the Rel/NF-κB family. We have previously shown that c-rel mRNAs accumulate in different types of apoptotic cells of the chick embryo, especially in mesenchymal cells within the four cell death areas of the limb bud: the anterior and posterior necrotic zones, the opaque patch and the interdigital necrotic zones. This study aimed to further establish the involvement of c-Rel in apoptosis of the developing limb by investigating its expression in the talpid3 mutant which was originally shown to be defective in apoptosis. However, our preliminary examinations highlighted the apparent presence of apoptotic cells in talpid3 embryos. Hence, we performed a systematic study of the occurence of apoptosis in mutant and control embryos by the TUNEL method. The results revealed that apoptosis does occur in talpid3 embryos but with altered spatial and temporal patterns. This suggests that the talpid3 mutation does not affect a gene involved in apoptosis per se but rather in the determination of the pattern of apoptosis. Neither the expression of c-Rel nor that of its IκBα inhibitor are grossly modified in talpid3 limb buds, suggesting that the talpid3 mutation does not affect any of these genes. They are mostly expressed in epidermal, endodermal and striated muscle cells in control and in talpid3 limb buds as well. C-Rel was also detected in some scarce mesenchymal cells that could be apoptotic, in both control and mutant embryos. The only slight difference between control and talpid3 limbs lies in the perichondrium which is not fully differentiated in talpid3 embryos: c-Rel and IκBα are only faintly expressed in talpid3 perichondrial cells, whereas they are both detected in control perichondrial cells. Taken together, these results suggest that c-Rel could participate in several developmental processes, especially in the differentiation of perichondrial cells, besides its already documented involvement in apoptosis and haematopoeisis.

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References

  1. Golstein P. Controlling cell death. Science 1997; 275: 1081-1082.

    Google Scholar 

  2. Green DR, Reed JC. Mitochondria and apoptosis. Science 1998; 281: 1309-1312.

    Google Scholar 

  3. Thornberry NA, Lazebnik Y. Caspases: enemies within. Science 1998; 281: 1312-1316.

    Google Scholar 

  4. Adams JM, Cory S. The Bcl-2 family: arbiters of cell death. Science 1998; 281: 1322-1326.

    Google Scholar 

  5. Hale AJ, Smith CA, Sutherland LC, et al. Apoptosis: molecular regulation of cell death. Eur J Biochem 1996; 236: 1-26.

    Google Scholar 

  6. Bossy-Wetzel E, Bakiri L, Yaniv M. Induction of apoptosis by the transcription factor c-Jun. EMBO J 1997; 16: 1695-1709.

    Google Scholar 

  7. Evan G, Littlewood T. A matter of life and cell death. Science 1998; 281: 1317-1322.

    Google Scholar 

  8. Baichwal VR, Baeuerle PA. Apoptosis: activate NF-κB or die? Curr Biol 1997; 7: R94-R96.

    Google Scholar 

  9. Abbadie C, Kabrun N, Bouali F, et al. High levels of c-rel expression are associated with programmed cell death in the developing avian embryo and in bone marrow cells in vitro. Cell 1993; 75: 899-912.

    Google Scholar 

  10. Hinchliffe JR, Thorogood PV. Genetic inhibition of mesenchymal cell death and the development of form and skeletal pattern in the limbs of talpid3 (ta3) mutant chick embryos. J Embryol Exp Morph 1974; 31: 747-760.

    Google Scholar 

  11. Hunton P. A study of some factors affecting the hatchability of chicken eggs, with special reference to genetic control. [MSc Thesis] Wye College, University of London. 1960.

  12. Hinchliffe JR, Ede DA. Limb development in the polydactylous talpid3 mutant of the fowl. J Embryol Exp Morph 1967; 17: 285-404.

    Google Scholar 

  13. Gavrieli Y, Sherman Y, Ben-Sasson SA. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 1992; 119: 493-501.

    Google Scholar 

  14. Morrison LE, Kabrun N, Mudri S, Hayman MJ, Enrietto PJ. Viral rel and cellular rel associate with cellular proteins in transformed and normal cells. Oncogene 1989; 4: 677-683.

    Google Scholar 

  15. Davis JN, Bargmann W, Bose HJ. Identification of protein complexes containing the c-rel proto-oncogene product in avian hematopoietic cells. Oncogene 1990; 5: 1109-1115.

    Google Scholar 

  16. Kerr LD, Inoue J, Davis N, et al. The rel-associated pp40 protein prevents DNA binding of Rel and NF-kappa B: relationship with I kappa B beta and regulation by phosphorylation. Genes Dev 1991; 5: 1464-1476.

    Google Scholar 

  17. Kochel T, Mushinski JF, Rice NR. The v-Rel and c-Rel proteins exist in high molecular weight complexes in avian and murine cells. Oncogene 1991; 6: 615-626.

    Google Scholar 

  18. Schatzle JD, Kralova J, Bose HR. Avian IκBα is transcriptionally induced by c-Rel and v-Rel with different kinetics. J Virol 1995; 69: 5383-5390.

    Google Scholar 

  19. Hrdlickova R, Nehyba J, Humphries EH. v-rel induces expression of three avian immunoregulatory surface receptors more efficiently than c-rel. J Virol 1994; 68: 308-319.

    Google Scholar 

  20. Miyamoto S, Verma IM. Rel/NF-κB/IκB story. Adv Cancer Res 1995; 66: 255-292.

    Google Scholar 

  21. Huguet C, Mattot V, Bouali F, et al. The avian transcription factor c-Rel is induced and translocates into the nucleus of thymocytes undergoing apoptosis. Cell Death and Diff 1997; 4: 413-422.

    Google Scholar 

  22. Wulczyn FG, Krappmann D, Scheidereit C. The NF-κB/Rel and IκB gene families: mediators of immune response and inflammation. J Mol Med 1996; 74: 749-769.

    Google Scholar 

  23. Bushdid PB, Brantley DM, Yull FE, et al. Inhibition of NF-κB activity results in disruption of the apical ectodermal ridge and aberrant limb morphogenesis. Nature 1998; 392: 615-618.

    Google Scholar 

  24. Kanegae Y, Tavares AT, Izpisua Belmonte JC, Verma IM. Role of Rel/NF-κB transcription factors during the outgrowth of the vertebrate limb. Nature 1998; 392: 611-614.

    Google Scholar 

  25. Ede DA, Kelly WA. Developmental abnormalities in the trunk and limbs of the talpid3 mutant of the fowl. J Embryol Exp Morph 1964b; 12: 339-356.

    Google Scholar 

  26. Ganan Y, Macias D, Duterque-Coquillaud M, Ros MA, Hurle JM. Role of TGFβs and BMPs as signals controlling the position of the digits and the areas of interdigital cell death in the developping chick limb autopod. Development 1996; 122: 2349-2357.

    Google Scholar 

  27. Zou H, Niswander L. Requirement for BMP signaling in interdigital apoptosis and scale formation. Science 1996; 272: 738-741.

    Google Scholar 

  28. Yokouchi Y, Sakiyama J, Kameda T, et al. BMP-2/-4 mediate programmed cell death in chicken limb buds. Development 1996; 122: 3725-3734.

    Google Scholar 

  29. Francis-West PH, Robertson KE, Ede DA, et al. Expression of genes encoding Bone Morphogenetic Proteins and Sonic Hedgehog in talpid3 limb buds: their relationships in the signalling cascade involved in limb patterning. Dev Dyn 1995; 203: 187-197.

    Google Scholar 

  30. Cox KH, DeLeon DV, Angerer LM, Angerer RC. Detection of mRNAs in sea urchin embryos by in situ hybridization using asymmetric RNA probes. Dev Biol 1984; 101: 485-502.

    Google Scholar 

  31. Quéva C, Ness SA, Graf T, Vandenbunder B, Stéhelin D. Expression patterns of c-myb and of v-myb induced myeloid-1 (mim-1) gene during the development of the chick embryo. Development 1992; 114: 125-133.

    Google Scholar 

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Huguet, C., Morrice, D.R., Bouali, F. et al. Expression of transcription factor c-Rel and apoptosis occurrence in polydactylous and syndactylous limb buds of the talpid3 mutant chick embryo. Apoptosis 4, 31–38 (1999). https://doi.org/10.1023/A:1009678015249

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