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Sonic Hedgehog Signalling in the Developing and Regenerating Fins of Zebrafish

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Shh and Gli Signalling and Development

Part of the book series: Molecular Biology Intelligence Unit ((MBIU))

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Abstract

Zebrafish is now a well established model for the study of developmental and regenerative processes. Indeed, the genetic cascades that control the early development of the structure that will form the paired fins (the fin bud) present similarities with the early formation of the tetrapod fore and hindlimb buds. One of these conserved molecular pathways involves secreted factors of the Hedgehog family [sonic hedgehog (shh) and tiggywinkle hedgehog (twhh)]. As in the tetrapod limbs, hedgehog proteins are initially expressed in the posterior region of the early fin bud where they contribute to the patterning of the antero-posterior axis, then are involved in cell proliferation and the formation of various skeletal elements. The hedgehog pathway is reactivated in adult fish following fin amputation, an event that triggers the regeneration program. During this process, the hedgehog signal is involved in various processes such as the growth and maintenance of the blastema and patterning of the fin ray.

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References

  1. Krauss S, Concordet JP, Ingham PW. A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos. Cell 1993; 75(7):1431–1444.

    Article  PubMed  CAS  Google Scholar 

  2. Ekker SC, Ungar AR, Greenstein P et al. Patterning activities of vertebrate hedgehog proteins in the developing eye and brain. Curr Biol 1995; 5(8):944–955.

    Article  PubMed  CAS  Google Scholar 

  3. Currie PD, Ingham PW. Induction of a specific muscle cell type by a hedgehog-like protein in zebrafish. Nature 1996; 382(6590):452–455.

    Article  PubMed  CAS  Google Scholar 

  4. Avaron F, Hoffman L, Guay D et al. Characterization of two new zebrafish members of the hedgehog family: atypical expression of the zebrafish indian hedgehog gene in skeletal elements of both endochondral and dermal origins. Dev Dyn 2006; 235(2):478–89.

    Article  PubMed  CAS  Google Scholar 

  5. Dane PJ, Tucker JB. Modulation of epidermal cell shaping and extracellular matrix during caudal fin morphogenesis in the zebra fish Brachydanio rerio. J Embryol Exp Morphol 1985; 87:145–161.

    PubMed  CAS  Google Scholar 

  6. Grandel H, Schulte-Merker S. The development of the paired fins in the zebrafish (Danio rerio). Mech Dev 1998; 79(1–2):99–120.

    Article  PubMed  CAS  Google Scholar 

  7. Akimenko MA, Ekker M. Anterior duplication of the Sonic hedgehog expression pattern in the pectoral fin buds of zebrafish treated with retinoic acid. Dev Biol 1995; 170(1):243–247.

    Article  PubMed  CAS  Google Scholar 

  8. Riddle RD, Johnson RL, Laufer E et al. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 1993; 75(7):1401–1416.

    Article  PubMed  CAS  Google Scholar 

  9. Fallon JF, Lopez A, Ros MA et al. FGF-2: Apical ectodermal ridge growth signal for chick limb development. Science 1994; 264:104–107.

    Article  PubMed  CAS  Google Scholar 

  10. Vogel A, Rodriguez C, IzpisĂºa-Belmonte J-C. Involvement of FGF-8 in initiation, outgrowth and patterning of the vertebrate limb. Development 1996; 122:1737–1750.

    PubMed  CAS  Google Scholar 

  11. Loomis CA, Harris E, Michaud J et al. The mouse Engrailed-1 gene and ventral limb patterning. Nature 1996; 382:360–363.

    Article  PubMed  CAS  Google Scholar 

  12. Riddle RD, Ensini M, Nelson C et al. Induction of the LIM homeobox gene Lmx1 by WNT7a establishes dorsoventral pattern in the vertebrate limb. Cell 1995; 83:631–640.

    Article  PubMed  CAS  Google Scholar 

  13. Bruneau S, Rosa FM. Dynamo, a new zebrafish DVR member of the TGF-beta superfamily is expressed in the posterior neural tube and is up-regulated by Sonic hedgehog. Mech Dev 1997; 61(1–2):199–212.

    Article  PubMed  CAS  Google Scholar 

  14. Hoffman L, Miles J, Avaron F et al. Exogenous retinoic acid induces a stage-specific, transient and progressive extension of Sonic hedgehog expression across the pectoral fin bud of zebrafish. Int J Dev Biol 2002; 46(7):949–956.

    PubMed  CAS  Google Scholar 

  15. Laforest L, Brown CW, Poleo G et al. Involvement of the sonic hedgehog, patched 1 and bmp2 genes in patterning of the zebrafish dermal fin rays. Development 1998; 125(21):4175–4184.

    PubMed  CAS  Google Scholar 

  16. Chandrasekhar A, Warren Jr JT, Takahashi K et al. Role of sonic hedgehog in branchiomotor neuron induction in zebrafish. Mech Dev 1998; 76(1–2):101–115.

    Article  PubMed  CAS  Google Scholar 

  17. Du SJ, Dienhart M. Zebrafish tiggy-winkle hedgehog promoter directs notochord and floor plate green fluorescence protein expression in transgenic zebrafish embryos. Dev Dyn 2001; 222(4):655–666.

    Article  PubMed  CAS  Google Scholar 

  18. Ng JK, Tamura K, Buscher D et al. Molecular and cellular basis of pattern formation during vertebrate limb development. Curr Top Dev Biol 1999; 41:37–66.

    Article  PubMed  CAS  Google Scholar 

  19. Capdevila J, Izpisua Belmonte JC. Patterning mechanisms controlling vertebrate limb development. Annu Rev Cell Dev Biol 2001; 17:87–132.

    Article  PubMed  CAS  Google Scholar 

  20. Lu H-C, Revelli J-P, Goering L et al. Retinoid signaling is required for the establishment of a ZPA and for the expression of Hoxb-8, a mediator of ZPA formation. Development 1997; 124:1643–1651.

    PubMed  CAS  Google Scholar 

  21. Helms J, Thaller C, Eichele G. Relationship between retinoic acid and sonic hedgehog, two polarizing signals in the chick wing bud. Development 1994; 120:3267–3274.

    PubMed  CAS  Google Scholar 

  22. Tickle C, Alberts BM, Wolpert L et al. Local application of retinoic acid to the limb bud mimics the action of the polarizing region. Nature 1982; 296:564–565.

    Article  PubMed  CAS  Google Scholar 

  23. Chang DT, Lopez A, von Kessler DP et al. Products, genetic linkage, and limb patterning activity of a murine hedgehog gene. Development 1994; 120:3339–3353.

    PubMed  CAS  Google Scholar 

  24. Neumann CJ, Grandel H, Gaffield W et al. Transient establishment of anteroposterior polarity in the zebrafish pectoral fin bud in the absence of sonic hedgehog activity. Development 1999; 126(21):4817–4826.

    PubMed  CAS  Google Scholar 

  25. Chang B-E, Blader P, Fischer N et al. Axial (HNF3β) and retinoic acid receptors are regulators of the zebrafish sonic hedgehog promoter. EMBO J 1997; 16:3955–3964.

    Article  PubMed  CAS  Google Scholar 

  26. Schauerte HE, van Eeden FJ, Fricke C et al. Sonic hedgehog is not required for the induction of medial floor plate cells in the zebrafish. Development 1998; 125(15):2983–2993.

    PubMed  CAS  Google Scholar 

  27. van Eeden FJ, Granato M, Schach U et al. Mutations affecting somite formation and patterning in the zebrafish, Danio rerio. Development 1996; 123:153–164.

    PubMed  Google Scholar 

  28. Barresi MJ, Stickney HL, Devoto SH. The zebrafish slow-muscle-omitted gene product is required for Hedgehog signal transduction and the development of slow muscle identity. Development 2000; 127(10):2189–2199.

    PubMed  CAS  Google Scholar 

  29. van Eeden FJM, Granato M, Schach U et al. Genetic analysis of fin formation in the zebrafish, Danio rerio. Development 1996; 123:255–262.

    PubMed  Google Scholar 

  30. Grandel H, Draper BW, Schulte-Merker S. Dackel acts in the ectoderm of the zebrafish pectoral fin bud to maintain AER signaling. Development 2000; 127(19):4169–4178.

    PubMed  CAS  Google Scholar 

  31. Borday V, Thaeron C, Avaron F et al. Evx1 transcription in bony fin rays segment boundaries leads to a reiterated pattern during zebrafish fin development and regeneration. Dev Dynamics 2001; 220:91–98.

    Article  CAS  Google Scholar 

  32. Johnson SL, Weston JA. Temperature-sensitive mutations that cause stage-specific defects in zebrafish fin regeneration. Genetics 1995; 141:1583–1595.

    PubMed  CAS  Google Scholar 

  33. Poss KD, Keating MT, Nechiporuk A. Tales of regeneration in zebrafish. Dev Dynamics 2003; 226(2):202–210.

    Article  Google Scholar 

  34. Poss KD, Shen J, Nechiporuk A et al. Roles for Fgf signaling during zebrafish fin regeneration. Dev Biol 2000; 222(2):347–358.

    Article  PubMed  CAS  Google Scholar 

  35. Akimenko MA, Mari-Beffa M, Becerra J et al. Old questions, new tools, and some answers to the mystery of fin regeneration. Dev Dynamics 2003; 226(2):190–201.

    Article  Google Scholar 

  36. Poleo G, Brown CW, Laforest L et al. Cell proliferation and movement during earlin fin regeneration in zebrafish. Dev Dynamics 2001; 221:380–390.

    Article  CAS  Google Scholar 

  37. Nechiporuk A, Keating MT. A proliferation gradient between proximal and msxb-expressing distal blastema directs zebrafish fin regeneration. Development 2002; 129(11):26O7–2617.

    Google Scholar 

  38. Akimenko M-A, Johnson SL, Westerfield M et al. Differential induction of four msx homeobox genes during fin development and regeneration in zebrafish. Development 1995; 121:347–357.

    PubMed  CAS  Google Scholar 

  39. Poss KD, Shen J, Keating MT. Induction of lef1 during zebrafish fin regeneration. Dev Dyn 2000; 219(2):282–286.

    Article  PubMed  CAS  Google Scholar 

  40. Santamaría JA, Marí-Beffa M, Santos-Ruiz L et al. Incorporation of bromodeoxyuridine in regenerating fin tissue of the goldfish Carassius auratus. J Exp Zool 1996; 275:300–307.

    Article  PubMed  Google Scholar 

  41. St-Jacques B, Hammerschmidt M, McMahon AP. Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev 1999; 13(16):2072–2086.

    Article  PubMed  CAS  Google Scholar 

  42. Vortkamp A, Lee K, Lanske B et al. Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 1996; 273(5275):613–622.

    Article  PubMed  CAS  Google Scholar 

  43. Quint E, Smith A, Avaron F et al. Bone patterning is altered in the regenerating zebrafish caudal fin after ectopic expression of sonic hedgehog and bmp2b or exposure to cyclopamine. Proc Natl Acad Sci USA 2002; 99(13):8713–8718.

    PubMed  CAS  Google Scholar 

  44. Poss KD, Nechiporuk A, Hillam AM et al. Mps1 defines a proximal blastemal proliferative compartment essential for zebrafish fin regeneration. Development 2002; 129(22):5l41–5149.

    Google Scholar 

  45. Géraudie J, Brulfert A, Monnot M-J et al. Teratogenic and morphogenetic effects of retinoic acid on the regenerating pectoral fin in zebrafish. J Exp Zool 1994; 269:12–22.

    Article  Google Scholar 

  46. Canalis E, Economides AN, Gazzerro E. Bone morphogenetic proteins, their antagonists, and the skeleton. Endocr Rev 2003; 24(2):218–235.

    Article  PubMed  CAS  Google Scholar 

  47. Yoon BS, Lyons KM. Multiple functions of BMPs in chondrogenesis. J Cell Biochem 2004; 93(1):93–103.

    Article  PubMed  CAS  Google Scholar 

  48. Piccolo S, Sasai Y, Lu B et al. Dorsoventral patterning in Xenopus: Inhibition of ventral signals by direct binding of chordin to BMP-4. Cell 1996; 86(4):589–598.

    Article  PubMed  CAS  Google Scholar 

  49. Incardona JP, Gaffield W, Kapur RP et al. The teratogenic Veratrum alkaloid cyclopamine inhibits sonic hedgehog signal transduction. Development 1998; 125(18):3553–3562.

    PubMed  CAS  Google Scholar 

  50. Nechiporuk A, Poss KD, Johnson SL et al. Positional cloning of a temperature-sensitive mutant emmental reveals a role for sly1 during cell proliferation in zebrafish fin regeneration. Dev Biol 2003; 258(2):291–306.

    Article  PubMed  CAS  Google Scholar 

  51. Fischer S, Draper BW, Neumann CJ. The zebrafish fgf24 mutant identifies an additional level of Fgf signaling involved in vertebrate forelimb initiation. Development 2003; 130(15):3515–3524.

    Article  PubMed  CAS  Google Scholar 

  52. Nusse R. Wnts and Hedgehogs: Lipid-modified proteins and similarities in signaling mechanisms at the cell surface. Development 2003; 130(22):5297–5305.

    Article  PubMed  CAS  Google Scholar 

  53. Watt FM. Unexpected Hedgehog-Wnt interactions in epithelial differentiation. Trends Mol Med 2004; 10(12):577–580.

    Article  PubMed  CAS  Google Scholar 

  54. Callahan CA, Oro AE. Monstrous attempts at adnexogenesis: Regulating hair follicle progenitors through Sonic hedgehog signaling. Curr Opin Genet Dev 2001; 11(5):541–546.

    Article  PubMed  CAS  Google Scholar 

  55. Robertson CP, Braun MM, Roelink H. Sonic hedgehog patterning in chick neural plate is antagonized by a Wnt3-like signal. Dev Dyn 2004; 229(3):510–519.

    Article  PubMed  CAS  Google Scholar 

  56. Hu H, Hilton MJ, Tu X et al. Sequential roles of Hedgehog and Wnt signaling in osteoblast development. Development 2005; 132(1):49–60.

    Article  PubMed  CAS  Google Scholar 

  57. Karlstrom RO, Talbot WS, Schier AF. Comparative synteny cloning of zebrafish you-too: Mutations in the Hedgehog target gli2 affect ventral forebrain patterning. Genes Dev 1999; 13(4):388–393.

    Article  PubMed  CAS  Google Scholar 

  58. Nakano Y, Kim HR, Kawakami A et al. Inactivation of dispatched 1 by the chameleon mutation disrupts Hedgehog signalling in the zebrafish embryo. Dev Biol 2004; 269(2):381–392.

    Article  PubMed  CAS  Google Scholar 

  59. Baxendale S, Davison C, Muxworthy C et al. The B-cell maturation factor Blimp-1 specifies vertebrate slow-twitch muscle fiber identity in response to Hedgehog signaling. Nat Genet 2004; 36(1):88–93.

    Article  PubMed  CAS  Google Scholar 

  60. Varga ZM, Amores A, Lewis KE et al. Zebrafish smoothened functions in ventral neural tube specification and axon tract formation. Development 2001; 128(18):3497–3509.

    PubMed  CAS  Google Scholar 

  61. Sekimizu K, Nishioka N, Sasaki H et al. The zebrafish iguana locus encodes Dzip1, a novel zinc-finger protein required for proper regulation of Hedgehog signaling. Development 2004; 131(11):2521–2532.

    Article  PubMed  CAS  Google Scholar 

  62. Karlstrom RO, Tyurina OV, Kawakami A et al. Genetic analysis of zebrafish gli1 and gli2 reveals divergent requirements for gli genes in vertebrate development. Development 2003; 130(8):1549–1564.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Medicine and Cellular and Molecular Medicine, Ottawa Health Research Institute, University of Ottawa, 725 Parkdale Avenue, Ottawa, ON, K1Y4E9, Canada

    Fabien Avaron, Amanda Smith & Marie-Andrée Akimenko

Authors
  1. Fabien Avaron
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  2. Amanda Smith
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  3. Marie-Andrée Akimenko
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© 2006 Landes Bioscience and Springer Science+Business Media

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Avaron, F., Smith, A., Akimenko, MA. (2006). Sonic Hedgehog Signalling in the Developing and Regenerating Fins of Zebrafish. In: Shh and Gli Signalling and Development. Molecular Biology Intelligence Unit. Springer, New York, NY. https://doi.org/10.1007/978-0-387-39957-7_9

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