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Evidence that the canonical Wnt signalling pathway regulates deer antler regeneration

  1. J. G. Mount,
  2. M. Muzylak,
  3. S. Allen,
  4. T. Althnaian,
  5. I. M. McGonnell,
  6. J. S. Price*

Article first published online: 21 MAR 2006

DOI: 10.1002/dvdy.20742

Issue

Developmental Dynamics

Developmental Dynamics

Special Issue: Craniofacial Development Special Issue

Volume 235, Issue 5, pages 1390–1399, May 2006

Additional Information

How to Cite

Mount, J. G., Muzylak, M., Allen, S., Althnaian, T., McGonnell, I. M. and Price, J. S. (2006), Evidence that the canonical Wnt signalling pathway regulates deer antler regeneration. Dev. Dyn., 235: 1390–1399. doi: 10.1002/dvdy.20742

Author Information

  1. Department of Veterinary Basic Sciences, Royal Veterinary College, London, United Kingdom

*Department of Veterinary Basic Sciences, The Royal Veterinary College, Royal College Street, Camden, London, NW1 OUT, UK

Publication History

  1. Issue published online: 19 APR 2006
  2. Article first published online: 21 MAR 2006
  3. Manuscript Accepted: 13 FEB 2006

Funded by

  • BBSRC

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REFERENCES

  • Althnaian T, Allen SP, Muzylak M, Mount JM, Price JS. 2004. Activation of the Wnt signalling pathway inhibits osteoclast differentiation and bone resorption. J Bone Miner Res 19: S281.
  • Babij P, Zhao W, Small C, Kharode Y, Yaworsky PJ, Bouxsein ML, Reddy PS, Bodine PV, Robinson JA, Bhat B, Marzolf J, Moran RA, Bex F. 2003. High bone mass in mice expressing a mutant LRP5 gene. J Bone Miner Res 18: 960–974.
    Direct Link:
  • Bain G, Muller T, Wang X, Papkoff J. 2003. Activated β-catenin induces osteoblast differentiation of C3H10T1/2 cells and participates in BMP2 mediated signal transduction. Biochem Biophys Res Commun 301: 84–91.
  • Bode H. 2003. Head regeneration in Hydra. Dev Dyn 226: 225–236.
    Direct Link:
  • Bodine PV, Komm BS. 2002. Tissue culture models for studies of hormone and vitamin action in bone cells. Vitam Horm 64: 101–151.
  • Brault V, Moore R, Kutsch S, Ishibashi M, Rowitch D, McMahon A, Sommer L, Boussadia O, Kemler R. 2001. Inactivation of the (beta)-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 128: 1253–1264.
  • Brockes JP. 1997. Amphibian limb regeneration: rebuilding a complex structure. Science 276: 81–87.
  • Cadigan KM, Nusse R. 1997. Wnt signaling: a common theme in animal development. Genes Dev 11: 3286–3305.
  • Canalis E, Deregowski V, Pereira RC, Gazzerro E. 2005. Signals that determine the fate of osteoblastic cells. J Endocrinol Invest 28: 3–7.
  • Caubit X, Nicolas S, Le Parco Y. 1997. Possible roles for Wnt genes in growth and axial patterning during regeneration of the tail in urodele amphibians. Dev Dyn 210: 1–10.
    Direct Link:
  • Church V, Nohno T, Linker C, Marcelle C, Francis-West P. 2002. Wnt regulation of chondrocyte differentiation. J Cell Sci 115: 4809–4818.
  • Colitti M, Allen SP, Price JS. 2005. Programmed cell death in the regenerating deer antler. J Anat 207: 339–351.
    Direct Link:
  • Dashwood WM, Orner GA, Dashwood RH. 2002. Inhibition of beta-catenin/Tcf activity by white tea, green tea, and epigallocatechin-3-gallate (EGCG): minor contribution of H(2)O(2) at physiologically relevant EGCG concentrations. Biochem Biophys Res Commun 296: 584–588.
  • Day TF, Guo X, Garrett-Beal L, Yang Y. 2005. Wnt/beta-catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis. Dev Cell 8: 739–750.
  • de Boer J, Siddappa R, Gaspar C, Apeldoorn A, Fodde R, van Blitterwijk A. 2004. Wnt signalling inhibits osteogenic differentiation of human mesenchymal stem cells. Bone 34: 818–826.
  • Dorsky RI, Moon RT, Raible DW. 1998. Control of neural crest cell fate by the Wnt signalling pathway. Nature 396: 370–373.
  • Enomoto-Iwamoto M, Kitagaki J, Koyama E, Tamamura Y, Wu C, Kanatani N, Koike T, Okada H, Komori T, Yoneda T. 2002. The Wnt antagonist Frzb-1 regulates chondrocyte maturation and long bone development during limb skeletogenesis. Dev Biol 251: 142–156.
  • Faucheux C, Nesbitt SA, Horton MA, Price JS. 2001. Cells in regenerating deer antler cartilage provide a microenvironment that supports osteoclast differentiation. J Exp Biol 204: 443–455.
  • Faucheux C, Nicholls BM, Allen S, Danks JA, Horton MA, Price JS. 2004. Recapitulation of the parathyroid hormone-related peptide-Indian hedgehog pathway in the regenerating deer antler. Dev Dyn 231: 88–97.
    Direct Link:
  • Gavrieli Y, Sherman Y, Ben-Sasson SA. 1992. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119: 493–501.
  • Glass DA, 2nd, Bialek P, Ahn JD, Starbuck M, Patel MS, Clevers H, Taketo MM, Long F, McMahon AP, Lang RA, Karsenty G. 2005. Canonical Wnt signaling in differentiated osteoblasts controls osteoclast differentiation. Dev Cell 8: 751–764.
  • Gong Y, Slee RB, Fukai N, Rawadi G, Roman-Roman S, Reginato AM, Wang H, Cundy T, Glorieux FH, Lev D, Zacharin M, Oexle K, Marcelino J, Suwairi W, Heeger S, Sabatakos G, Apte S, Adkins WN, Allgrove J, Arslan-Kirchner M, Batch JA, Beighton P, Black GC, Boles RG, Boon LM, Borrone C, Brunner HG, Carle GF, Dallapiccola B, De Paepe A, Floege B, Halfhide ML, Hall B, Hennekam RC, Hirose T, Jans A, Juppner H, Kim CA, Keppler-Noreuil K, Kohlschuetter A, LaCombe D, Lambert M, Lemyre E, Letteboer T, Peltonen L, Ramesar RS, Romanengo M, Somer H, Steichen-Gersdorf E, Steinmann B, Sullivan B, Superti-Furga A, Swoboda W, van den Boogaard MJ, Van Hul W, Vikkula M, Votruba M, Zabel B, Garcia T, Baron R, Olsen BR, Warman ML. 2001. LDL receptor-related protein 5 (LRP5) affects bone accrual and eye development. Cell 107: 513–523.
  • Grotewold L, Ruther U. 2002. Bmp, Fgf and Wnt signalling in programmed cell death and chondrogenesis during vertebrate limb development: the role of Dickkopf-1. Int J Dev Biol 46: 943–947.
  • Hadjiargyrou M, Lombardo F, Zhao S, Ahrens W, Joo J, Ahn H, Jurman M, White DW, Rubin CT. 2002. Transcriptional Profiling of Bone Regeneration: Insight into the molecular complexity f wound repair. J Biol Chem 277: 30177–30182.
  • Haq S, Michael A, Andreucci M, Bhattacharya K, Dotto P, Walters B, Woodgett J, Kilter H, Force T. 2003. Stabilization of beta -catenin by a Wnt-independent mechanism regulates cardiomyocyte growth. PNAS 100: 4610–4615.
  • Hari L, Brault V, Kleber M, Lee H-Y, Ille F, Leimeroth R, Paratore C, Suter U, Kemler R, Sommer L. 2002. Lineage-specific requirements of {beta}-catenin in neural crest development. J Cell Biol 159: 867–880.
  • Hartmann C, Tabin C. 2000. Dual roles of Wnt signaling during chondrogenesis in the chicken limb. Development 127: 3141–3159.
  • Hens JR, Wilson KM, Dann P, Chen X, Horowitz MC, Wysolmerski JJ. 2005. TOPGAL mice show that the canonical Wnt signaling pathway is active during bone development and growth and is activated by mechanical loading in vitro. J Bone Miner Res 20: 1103–1113.
    Direct Link:
  • Hill TP, Spater D, Taketo MM, Birchmeier W, Hartmann C. 2005. Canonical Wnt/beta-catenin signaling prevents osteoblasts from differentiating into chondrocytes. Dev Cell 8: 727–738.
  • Holmen SL, Zylstra CR, Mukherjee A, Sigler RE, Faugere M-C, Bouxsein ML, Deng L, Clemens TL, Williams BO. 2005. Essential role of {beta}-catenin in postnatal bone acquisition. J Biol Chem 280: 21162–21168.
  • Huxley J. 1932. Problems of relative growth. Dial Press.
  • Johnson ML, Harnish K, Nusse R, Van Hul W. 2004. LRP5 and Wnt signaling: a union made for bone. J Bone Miner Res 19: 1749–1757.
    Direct Link:
  • Karen E, Yates S, Richard GR. 2005. Wnt influence on chondrocyte differentiation and cartilage function. DNA Cell Biol 24: 446–457.
  • Kitagaki J, Iwamoto M, Liu J-G, Tamamura Y, Pacifci M, Enomoto-Iwamoto M. 2003. Activation of β-catenin-LEF/TCF signal pathway in chondrocytes stimulates ectopic endochondral ossification. Osteoarthrit Cartil 11: 36–43.
  • Lee H-Y, Kleber M, Hari L, Brault V, Suter U, Taketo MM, Kemler R, Sommer L. 2004. Instructive role of Wnt/{beta}-catenin in sensory fate specification in neural crest stem cells. Science 303: 1020–1023.
  • Levasseur R, Kato M, Patel M, Chan L, Karsenty G. 2001. Low bone mass, Low weight and abnormal eye vascularization in mice deficient in LRP5, the gene mutated in human osteoporosis pseudoglioma syndrome. J Bone Miner Res 16: S152.
  • Li C, Suttie JM, Clark DE. 2004. Morphological observation of antler regeneration in red deer (Cervus elaphus). J Morphol 262: 731–740.
    Direct Link:
  • Li C, Suttie JM, Clark DE. 2005. Histological examination of antler regeneration in red deer (Cervus elaphus). Anat Rec A Discov Mol Cell Evol Biol 282: 163–179.
  • Little RD, Carulli JP, Del Mastro RG, Dupuis J, Osborne M, Folz C, Manning SP, Swain PM, Zhao SC, Eustace B, Lappe MM, Spitzer L, Zweier S, Braunschweiger K, Benchekroun Y, Hu X, Adair R, Chee L, FitzGerald MG, Tulig C, Caruso A, Tzellas N, Bawa A, Franklin B, McGuire S, Nogues X, Gong G, Allen KM, Anisowicz A, Morales AJ, Lomedico PT, Recker SM, Van Eerdewegh P, Recker RR, Johnson ML. 2002. A mutation in the LDL receptor-related protein 5 gene results in the autosomal dominant high-bone-mass trait. Am J Hum Genet 70: 11–19.
  • Logan C, Nusse R. 2004. The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol. 20: 781–810.
  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. 1951. Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265–275.
  • Monga SPS, Mars WM, Pediaditakis P, Bell A, Mule K, Bowen WC, Wang X, Zarnegar R, Michalopoulos GK. 2002. Hepatocyte growth factor induces Wnt-independent nuclear translocation of {beta}-catenin after met-{beta}-catenin dissociation in hepatocytes. Cancer Res 62: 2064–2071.
  • Nusse R, Varmus HE. 1992. Wnt genes. Cell 69: 1073–1087.
  • Otto WR, Rao J. 2004. Tomorrow's skeleton staff: mesenchymal stem cells and the repair of bone and cartilage. Cell Proliferation 37: 97–110.
    Direct Link:
  • Polakis P. 2000. Wnt signaling and cancer. Genes Dev. 14: 1837–1851.
  • Poss KD, Shen J, Keating MT. 2000. Induction of lef1 during zebrafish fin regeneration. Dev Dyn 219: 282–286.
  • Price J, Allen S. 2004. Exploring the mechanisms regulating regeneration of deer antlers. Philos Trans R Soc Lond B Biol Sci 359: 809–822.
  • Price J, Faucheux C, Allen S. 2005. Deer antlers as a model of mammalian regeneration. In: SchattenGP, editor. Current topics in developmental biology. San Diego: Academic Press. p 1–48.
  • Price JS, Oyajobi BO, Oreffo RO, Russell RG. 1994. Cells cultured from the growing tip of red deer antler express alkaline phosphatase and proliferate in response to insulin-like growth factor-I. J Endocrinol 143: R9–16.
  • Price JS, Oyajobi BO, Nalin AM, Frazer A, Russell RG, Sandell LJ. 1996. Chondrogenesis in the regenerating antler tip in red deer: expression of collagen types I, IIA, IIB, and X demonstrated by in situ nucleic acid hybridization and immunocytochemistry. Dev Dyn 205: 332–347.
    Direct Link:
  • Rawadi G, Vayssiere B, Dunn F, Baron R, Roman-Roman S. 2003. BMP-2 controls alkaline phosphatase expression and osteoblast mineralization by a Wnt autocrine loop. J Bone Miner Res 18: 1842–1853.
    Direct Link:
  • Reya T, Clevers H. 2005. Wnt signalling in stem cells and cancer. Nature 434: 843–850.
  • Roman-Roman S, Shi DL, Stiot V, Hay E, Vayssiere B, Garcia T, Baron R, Rawadi G. 2003. Murine frizzled-1 behaves as an antagonist of the canonical Wnt/beta -catenin signaling. J Biol Chem 279: 5725–5733.
  • Rudnicki JA, Brown AMC. 1997. Inhibition of chondrogenesis by Wnt gene expression in vivo and in vitro. Dev Biol 185: 104–118.
  • Ryu JH, Kim SJ, Kim SH, Oh CD, Hwang SG, Chun CH, Oh SH, Seong JK, Huh TL, Chun JS. 2002. Regulation of the chondrocyte phenotype by beta-catenin. Development 129: 5541–5550.
  • Slack JM. 1980. The source of cells for regeneration. Nature 286: 760.
  • Stott NS, Jiang TX, Chuong CM. 1999. Successive formative stages of precartilaginous mesenchymal condensations in vitro: modulation of cell adhesion by Wnt-7A and BMP-2. J Cell Physiol 180: 314–324.
    Direct Link:
  • Tamamura Y, Otani T, Kanatani N, Koyama E, Kitagaki J, Komori T, Yamada Y, Costantini F, Wakisaka S, Pacifici M, Iwamoto M, Enomoto-Iwamoto M. 2005. Developmental regulation of Wnt/{beta}-catenin signals is required for growth plate assembly, cartilage integrity, and endochondral ossification. J Biol Chem 280: 19185–19195.
  • Tufan A, Tuan C, Rocky S. 2001. Wnt regulation of limb mesenchymal chondrogenesis is accompanied by altered N-cadherin-related functions. FASEB J 15: 1436–1438.
  • van Noort M, Meeldijk J, van der Zee R, Destree O, Clevers H. 2002. Wnt signaling controls the phosphorylation status of beta-catenin. J Biol Chem 277: 17901–17905.
  • Yang Y. 2003. Wnts and wing: Wnt signaling in vertebrate limb development and musculoskeletal morphogenesis. Birth Defects Res Part C Embryo Today 69: 305–317.
    Direct Link:
  • Zechner D, Fujita Y, Hülsken J, Müller T, Walther I, Taketo M, Crenshaw E, Birchmeier W, Birchmeier C. 2003. Beta-catenin signals regulate cell growth and the balance between progenitor cell expansion and differentiation in the nervous system. Dev Biol 258: 406–418.
  • Zhong N, Gersch R, Hadjiargyou M. 2004. Dishevelled is required for chondrocyte proliferation and differentiation. JBMR 19: S34.
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