Roux's archives of developmental biology

, Volume 204, Issue 7–8, pp 509–512 | Cite as

Nerve dependent sulphated glycosaminoglycan synthesis in limb regeneration of the newt Pleurodeles waltl

  • B. Boilly
  • H. Hondermarck
  • M. Oudghir
  • E. Deudon
  • Y. Boilly-Marer
Short Communication
Received:
Accepted:

Abstract

Denervation of the amputated limb of newts stops the regeneration process by decreasing blastema cell proliferation. We investigated the effect of the denervation on each of the two compartments (epidermal cap, mesenchyme) in mid-bud blastemas on the level of sulphated glycosaminoglycans (GAGS). Denervation resulted in an increase of about threefold in the incorporation of [35S] sulphate into mesenchyme GAGs but had no effect on the epidermal cap. The increase of GAG synthesis in the mesenchymal part of the blastema involved both heparan sulphates and chondroitin-dermatan sulphates. Gel filtration showed no change in GAGs size after denervation. These results confirm that the mesenchymal part of the mid-bud blastema is the main target of nerves and, as heparan sulphates are known to store acidic fibroblast growth factor (aFGF), a polypeptide found in the blastema (Boilly et al.. 1991), this suggest that the nerves' effect on glycosaminoglycans turnover could be implicated in the control of bioavailability of this growth factor in the blastema.

Key words

Limb regeneration Denervation Sulphated glycosaminoglycans Heparan sulphates Growth control 
This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Albert P, Boilly B, Courty J, Barritault D (1987) Stimulation in cell culture of mesenchymous cells of newt limb blastema by EDGF I or II (basic or acidic FGF). Cell Differ 21:63–68Google Scholar
  2. Angello JC, Hosick HL, Anderson LWW (1982) Glycosaminoglycan synthesis by a cell line (C1-S1) established from a preneoplastic mouse mammary outgrowth. Cancer Res 42:4975–4978Google Scholar
  3. Boilly B, Oudkhir M, Lassalle B (1985) Control of the blastemal cell cycle by the peripheral nervous system during new-limb regeneration: continuous labeling analysis. Biol Cell 55: 107–112Google Scholar
  4. Boilly B, Moustafa Y, Oudkhir M (1986) Image analysis of blastemal cell proliferation in the denervated limb regenerate of the newt. Differentiation 32:208–214Google Scholar
  5. Boilly B, Lheureux E, Boilly-Marer Y, Bart A (1990) Cell interactions and regeneration control. Int J Dev Biol 34:219–231Google Scholar
  6. Boilly B, Cavanaugh KP, Thomas D, Hondermarck H, Bryant SV, Bradshaw RA (1991) Acidic fibroblast growth factor is present in regenerating limb blastemas of axolotls and binds specifically to blastema tissues. Dev Biol 145:302–310Google Scholar
  7. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254Google Scholar
  8. Brockes JP, Kintner CR (1986) Glial growth and nerve-dependent proliferation in the regeneration in the blastema of Urodele amphibians. Cell 45:301–306Google Scholar
  9. Dresden MH (1969) Denervation effects on newt limb regeneration: DNA, RNA and protein synthesis. Dev Biol 19:311–320Google Scholar
  10. Gallagher JT, Turnbull JE (1992) Heparan sulphate in the binding and activation of basic fibroblast growth factor. Glycobiology 2:523–528Google Scholar
  11. Geraudie J, Singer M (1978) Nerve dependent macromolecular synthesis in the epidermis and blastema of the adult new-regenerate. J Exp Zool 203:455–460Google Scholar
  12. Hondermarck H, Courty J, Ledoux D, Blankeert V, Barritault D, Boilly B (1990) Evidence of high and low affinity binding sites for basic fibroblast growth factor in mouse placenta. Biochem Biophys Res Commun 169:272–281Google Scholar
  13. Hondermarck H, Boilly B (1992) Characterisation of fibroblast growth factor binding in regenerating limb blastemas of axolotls. In: Taban CH, Boilly B (eds) Keys for regeneration. (Monogr Dev Biol Basel, vol 23) Karger, pp 110–115Google Scholar
  14. Hondermarck H, Deudon E, Boilly B (1992) Embryonic brain-derived heparan sulfate inhibits cellular membrane binding and biological activity of basic fibroblast growth factor. Dev Brain Res 68:247–253Google Scholar
  15. Leppä S, Mali M, Miettinen HM, Jalkanen M (1992) Syndecan expression regulates cell morphology and growth of mouse mammary epithelial tumor cells. Proc Natl Acad Sci USA 89:932–936Google Scholar
  16. Linker A, Sampson P (1960) The enzymatic degradation of heparan sulfates. Biochem Biophys Acta 43:366–368Google Scholar
  17. Mali M, Elenius K, Miettinen HM, Jalkanen M (1993) Inhibition of basic fibroblast growth factor-induced growth promotion by overexpression of syndecan-1. J Biol Chem 268:24215–24222Google Scholar
  18. Mescher AL, Munain SL (1986) Changes in the extracellular matrix and glycosaminoglycan synthesis during the initiation of regeneration in adult newt forelimbs. Anat Rec 214:424–431Google Scholar
  19. Oudkhir M, Martelly L, Castagna M, Moraczewski J, Boilly B (1989) Protein kinase C activity during limb regeneration of Amphibians. In: Kiortsis V Koussoulakos S, Wallace H (eds) Recent trends in regeneration research. Plenum Press, New York, pp 69–79Google Scholar
  20. Rapraeger A, Yeaman C (1989) A quantitative solid-phase assay for identifying radiolabeled glycosaminoglycans in crude extracts. Anal Biochem 179:361–365Google Scholar
  21. Singer M (1974) Neurotrophic control of limb regeneration in the newt. Ann NY Acad Sci 228:308–322Google Scholar
  22. Singer M (1978) On the nature of neurotrophic phenomenom in urodele limb regeneration. Am Zool 18:829–841Google Scholar
  23. Smith GN, Toole BP, Gross J (1975) Hyaluronidase activity and glycosaminoglycan synthesis in the amputated newt limb: comparison of denervated, nonregenerating limbs with regenerates. Dev Biol 43:221–232Google Scholar
  24. Sonn JK, Solursh M (1993) Activity of protein kinase C during the differentiation of chick limb bud mesenchymal cells. Differentiation 53:155–162Google Scholar
  25. Tassava RA, Olsen CL (1985) Neurotrophic influences on cellular proliferation in urodele limb regeneration: in vivo experiments. In: Sicard RE (ed) Regulation of vertebrate limb regeneration. Oxford University Press, pp 81–92Google Scholar
  26. Toole BP, Gross J (1971) The extracellular matrix of the regenerating newt limb: synthesis and removal of hyaluronate prior to differentiation. Dev Biol 25:57–77Google Scholar
  27. Vanrapenbusch S, Lassalle B (1989) Effects of denervation on the extracellular collagen matrix of limb regenerate of the newt, Pleurodeles waldii. In: Kiortsis V, Koussoulakos S, Wallace H (eds) Recent trends in regeneration research. Plenum Press, New York, pp 217–227Google Scholar
  28. Wallace H (1981) Vertebrate limb regeneration. Wiley, New YorkGoogle Scholar

Copyright information

© Springer-Verlag 1995

Authors and Affiliations

  • B. Boilly
    • 1
  • H. Hondermarck
    • 1
  • M. Oudghir
    • 2
  • E. Deudon
    • 3
  • Y. Boilly-Marer
    • 4
  1. 1.Laboratoire de Biologie Cellulaire et Moléculaire du DéveloppementUniversité des Sciences et Technologies de LilleLilleFrance
  2. 2.Laboratoire de BiochimieUniversité de MarrakechMarrakech
  3. 3.Laboratoire de Biochimie INSERM U 402Faculté de Médicine Saint-AntoineParisFrance
  4. 4.Université des Sciences et Technologies de LilleLilleFrance

Personalised recommendations