DOI: 10.1073/pnas.94.17.9159. Expression of <i>Sonic hedgehog</i> gene in regenerating newt limb blastemas recapitulates that in developing limb buds

Expression of Sonic hedgehog gene in regenerating newt limb blastemas recapitulates that in developing limb buds

10.1073/pnas.94.17.9159

Crossref journal-article

Proceedings of the National Academy of Sciences

Proceedings of the National Academy of Sciences (341)

Abstract

This study aimed at characterizing the Sonic hedgehog ( shh ) gene in newt limbs, which encodes a signaling molecule of the zone of polarizing activity (ZPA) responsible for determining the anterior–posterior axis of the embryonic chicken and mouse limbs. The reverse transcription–PCR showed that adult newt regenerating limbs express shh genes. In situ hybridization experiments demonstrated that shh genes were expressed in mesenchymal cells of the posterior region of both embryonic buds and regenerating blastemas of newt limbs, strongly suggesting the presence of ZPA in these tissues. Experiments of the axial reversal graft of blastemas further supported this suggestion. The grafted blastemas regenerated supernumerary limbs, and this has been explained by three models: the polar coordinate model, the boundary model, and the polarizing zone model. In favor of the third model, the shh gene was expressed not only in the original region (new anterior region) of the graft, but also ectopically in the other region (new posterior region) of the same graft. This study implies that the regenerating limb blastema produces ZPA as the signaling center of the AP patterning as in the developing limb bud and, therefore, supports the notion that the limb regeneration recapitulates the limb development.

Bibliography

Imokawa, Y., & Yoshizato, K. (1997). Expression of Sonic hedgehog gene in regenerating newt limb blastemas recapitulates that in developing limbâbuds. Proceedings of the National Academy of Sciences, 94(17), 9159â9164.

Authors 2

Yutaka Imokawa (first)
Katsutoshi Yoshizato (additional)

References 41 Referenced 109

H Wallace Vertebrate Limb Regeneration (Wiley, Toronto, 1981). / Vertebrate Limb Regeneration by Wallace H (1981)
D L Stocum Molecular Biology Intelligence Unit: Wound Repair, Regeneration and Artificial Tissues (Springer, New York, 1995). / Molecular Biology Intelligence Unit: Wound Repair, Regeneration and Artificial Tissues by Stocum D L (1995)
10.1016/0092-8674(91)90612-3
10.1016/0092-8674(93)90626-2
10.1146/annurev.cb.10.110194.001005
10.1242/dev.120.11.3339
10.1016/0092-8674(94)90030-2
10.1038/371609a0
10.1016/S0960-9822(95)00156-4
10.1016/0092-8674(95)90297-X
10.1038/298369a0
10.1016/0012-1606(84)90273-2
10.1016/0012-1606(92)90152-7
10.1242/dev.121.6.1731
10.1002/j.1460-2075.1988.tb03325.x
10.1242/dev.111.2.489
M Beauchemin, P Savard Limb Development and Regeneration, eds J F Fallon, P F Goetinck, R O Kelly, D L Stocum (Wiley–Liss, New York), pp. 41–50 (1993). / Limb Development and Regeneration by Beauchemin M (1993)
10.1242/dev.117.4.1397
J W Saunders, M T Gasseling Epithelial–Mesenchymal Interactions: Ectodermal–Mesenchymal Interactions in the Origin of Limb Symmetry, eds R Fleischmajer, R E Billingham (Williams & Wilkins, Baltimore), pp. 78–97 (1968). / Epithelial–Mesenchymal Interactions: Ectodermal–Mesenchymal Interactions in the Origin of Limb Symmetry by Saunders J W (1968)
10.1016/0012-1606(77)90175-0
S D Thoms, J F Fallon J Embryol Exp Morphol 60, 33–55 (1980). / J Embryol Exp Morphol by Thoms S D (1980)
10.1126/science.948762
10.1126/science.212.4498.993
T Meinhardt Developmental Order: Its Origin and Regulation (Liss, New York), pp. 439–461 (1982). / Developmental Order: Its Origin and Regulation by Meinhardt T (1982)
T Meinhardt J Embryol Exp Morphol 76, 115–137 (1983). / J Embryol Exp Morphol by Meinhardt T (1983)
10.1242/dev.121.3.619
10.1038/254199a0
D L Stocum J Embryol Exp Morphol 71, 193–214 (1982). / J Embryol Exp Morphol by Stocum D L (1982)
10.1016/0012-1606(84)90272-0
S Papageorgiou, N Holder J Embryol Exp Morphol 74, 143–158 (1983). / J Embryol Exp Morphol by Papageorgiou S (1983)
M Maden, K Mustafa J Embryol Exp Morphol 84, 233–253 (1984). / J Embryol Exp Morphol by Maden M (1984)
N Holder, C Weekes J Embryol Exp Morphol 82, 217–239 (1984). / J Embryol Exp Morphol by Holder N (1984)
Y Imokawa, G Eguchi Int J Dev Biol 36, 407–412 (1992). / Int J Dev Biol by Imokawa Y (1992)
K Okada, M Ichikawa Annu Rep Exp Morphol 3, 1–16 (1947). / Annu Rep Exp Morphol by Okada K (1947)
10.1007/BF00575834
J Sambrook, E F Fritsch, T Maniatis Molecular Cloning: A Laboratory Manual (Cold Spring Harbor Lab. Press, 2nd Ed., Plainview, NY, 1989). / Molecular Cloning: A Laboratory Manual by Sambrook J (1989)
10.1006/bbrc.1996.0069
10.1016/0012-1606(75)90381-4
10.1111/j.1440-169X.1994.00357.x
10.1016/0012-1606(75)90128-1
10.1242/dev.122.8.2319

Dates

Type	When
Created	23 years, 1 month ago (July 26, 2002, 10:32 a.m.)
Deposited	3 years, 4 months ago (April 13, 2022, 2:20 p.m.)
Indexed	11 months, 2 weeks ago (Sept. 19, 2024, 10:52 a.m.)
Issued	28 years ago (Aug. 19, 1997)
Published	28 years ago (Aug. 19, 1997)
Published Online	28 years ago (Aug. 19, 1997)
Published Print	28 years ago (Aug. 19, 1997)

Funders 0

None

BibTeX

@article{Imokawa_1997, title={Expression of Sonic hedgehog gene in regenerating newt limb blastemas recapitulates that in developing limb buds}, volume={94}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.94.17.9159}, DOI={10.1073/pnas.94.17.9159}, number={17}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Imokawa, Yutaka and Yoshizato, Katsutoshi}, year={1997}, month=aug, pages={9159–9164} }

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