Notochord-derived hedgehog is essential for tail regeneration in Xenopus tadpole
Tóm tắt
Appendage regeneration in amphibians is regulated by the combinatorial actions of signaling molecules. The requirement of molecules secreted from specific tissues is reflected by the observation that the whole process of regeneration can be inhibited if a certain tissue is removed from the amputated stump. Interestingly, urodeles and anurans show different tissue dependencies during tail regeneration. The spinal cord is essential for tail regeneration in urodele but not in anuran larva, whereas the notochord but not the spinal cord is essential for tail regeneration in anuran tadpoles. Sonic hedgehog is one of the signaling molecules responsible for such phenomenon in axolotl, as hedgehog signaling is essential for overall tail regeneration and sonic hedgehog is exclusively expressed in the spinal cord. In order to know whether hedgehog signaling is involved in the molecular mechanism underlying the inconsistent tissue dependency for tail regeneration between anurans and urodeles, we investigated expression of hedgehog signal-related genes in the regenerating tail of Xenopus tadpole and examined the effect of the hedgehog signal inhibitor, cyclopamine, on the tail regeneration. In Xenopus, sonic hedgehog is expressed exclusively in the notochord but not in the spinal cord of the regenerate. Overall regeneration was severely impaired in cyclopamine-treated tadpoles. Notochord maturation in the regenerate, including cell alignment and vacuolation, and myofiber formation were inhibited. Proliferation of spinal cord cells in the neural ampulla and of mesenchymal cells was also impaired. As in the axolotl, hedgehog signaling is required for multiple steps in tail regeneration in the Xenopus tadpole, although the location of the Shh source is quite different between the two species. This difference in Shh localization is the likely basis for the differing tissue requirement for tail regeneration between urodeles and anurans.
Tài liệu tham khảo
Carlson BM: An Introduction To Regeneration. Principles Of Regenerative Biology. 2007, London: Academic, 1-30.
Beck CW, Izpisúa Belmonte JC, Christen B: Beyond early development: xenopus as an emerging model for the study of regenerative mechanisms. Dev Dyn. 2009, 238: 1226-1248.
Slack JMW, Lin G, Chen Y: The Xenopus tadpole: a new model for regeneration research. Cell Mol Life Sci. 2008, 65: 54-63.
Tanaka EM, Reddien PW: The cellular basis for animal regeneration. Dev Cell. 2011, 21: 172-185.
Mochii M, Taniguchi Y, Shikata I: Tail regeneration in the Xenopus tadpole. Dev Growth Differ. 2007, 49: 155-161.
Beck CW, Christen B, Slack JMW: Molecular pathways needed for regeneration of spinal cord and muscle in a vertebrate. Dev Cell. 2003, 5: 429-439.
Beck CW, Christen B, Barker D, Slack JMW: Temporal requirement for bone morphogenetic proteins in regeneration of the tail and limb of Xenopus tadpoles. Mech Dev. 2006, 123: 674-688.
Ho DM, Whitman M: TGF-beta signaling is required for multiple processes during Xenopus tail regeneration. Dev Biol. 2008, 315: 203-216.
Lin G, Slack JMW: Requirement for Wnt and FGF signaling in Xenopus tadpole tail regeneration. Dev Biol. 2008, 316: 323-335.
Lin G, Chen Y, Slack JMW: Transgenic analysis of signaling pathways required for Xenopus tadpole spinal cord and muscle regeneration. Anat Rec. 2012, 295: 1532-1540.
Sugiura T, Tazaki A, Ueno N, Watanabe K, Mochii M: Xenopus Wnt-5a induces an ectopic larval tail at injured site, suggesting a crucial role for noncanonical Wnt signal in tail regeneration. Mech Dev. 2009, 126: 56-67.
Taniguchi Y, Sugiura T, Tazaki A, Watanabe K, Mochii M: Spinal cord is required for proper regeneration of the tail in Xenopus tadpoles. Dev Growth Differ. 2008, 50: 109-120.
Schnapp E, Kragl M, Rubin L, Tanaka EM: Hedgehog signaling controls dorsoventral patterning, blastema cell proliferation and cartilage induction during axolotl tail regeneration. Development. 2005, 132: 3243-3253.
Caubit X, Nicolas S, Shi DL, Le Parco Y: Reactivation and graded axial expression pattern of Wnt-10a gene during early regeneration stages of adult tail in amphibian urodele Pleurodeles waltl. Dev Dyn. 1997, 208: 139-148.
Caubit X, Nicolas S, Le Parco Y: Possible roles for Wnt genes in growth and axial patterning during regeneration of the tail in urodele amphibians. Dev Dyn. 1997, 210: 1-10.
Zhang F, Clarke JD, Ferretti P: FGF-2 Up-regulation and proliferation of neural progenitors in the regenerating amphibian spinal cord in vivo. Dev Biol. 2000, 225: 381-391.
Zhang F, Clarke JD, Santos-Ruiz L, Ferretti P: Differential regulation of fibroblast growth factor receptors in the regenerating amphibian spinal cord in vivo. Neuroscience. 2002, 114: 837-848.
Goldfarb AJ: The influence of the nervous system in regeneration. J Exp Zool. 1909, 7: 643-722.
Goss RJ: Principles of regeneration. 1969, New York: Academic
Géraudie J, Ferretti P: Gene expression during amphibian limb regeneration. Int Rev Cytol. 1998, 180: 1-50.
Holtzer H, Holtzer S, Avery G: An experimental analysis of the development of the spinal column. IV. Morphogenesis of tail vertebrae during regeneration. J Morph. 1955, 96: 145-168.
Takabatake T, Ogawa M, Takahashi TC, Mizuno M, Okamoto M, Takeshima K: Hedgehog and patched gene expression in adult ocular tissues. FEBS Lett. 1997, 410: 485-489.
Sugiura T, Taniguchi Y, Tazaki A, Ueno N, Watanabe K, Mochii M: Differential gene expression between the embryonic tail bud and regenerating larval tail in Xenopus laevis. Dev Growth Differ. 2004, 46: 97-105.
Chen Y, Lin G, Slack JMW: Control of muscle regeneration in the Xenopus tadpole tail by Pax7. Development. 2006, 133: 2303-2313.
Gargioli C, Slack JMW: Cell lineage tracing during Xenopus tail regeneration. Development. 2004, 131: 2669-2679.
Koleva M, Kappler R, Vogler M, Herwig A, Fulda S, Hahn H: Pleiotropic effects of sonic hedgehog on muscle satellite cells. Cell Mol Life Sci. 2005, 62: 1863-1870.
Elia D, Madhala D, Ardon E, Reshef R, Halevy O: Sonic hedgehog promotes proliferation and differentiation of adult muscle cells: Involvement of MAPK/ERK and PI3K/Akt pathways. Biochim Biophys Acta. 2007, 1773: 1438-1446.
Chiang C, Litingtung Y, Lee E, Young KE, Corden JL, Westphal H, Beachy PA: Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature. 1996, 383: 407-413.
Nieuwkoop PD, Faber J: Normal table of Xenopus laevis (daudin): a systematical and chronological survey of the development from the fertilized Egg till the End of metamorphosis. 1956, New York: Garland
Watanabe M, Frelinger AL, Rutishauser U: Topography of N-CAM structural and functional determinants. I. Classification of monoclonal antibody epitopes. J Cell Biol. 1986, 103: 1721-1727.
Kintner CR, Brockes JP: Monoclonal antibodies identify blastemal cells derived from dedifferentiating limb regeneration. Nature. 1984, 308: 67-69.
Kawakami A, Kimura-Kawakami M, Nomura T, Fujisawa H: Distributions of PAX6 and PAX7 proteins suggest their involvement in both early and late phases of chick brain development. Mech Dev. 1997, 66: 119-130.
NIBB/NIG/NBRP Xenopus laevis EST database (XDB3). [http://xenopus.nibb.ac.jp/]