Hedgehog signalling is required for perichondral osteoblast differentiation in zebrafish

Mechanisms of Development

Volumn 128, Issue 1-2, 2011, Pages 141-152

  Felber, Katharina ^a   Croucher, Peter ^b   Roehl, Henry H ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Bone; Cranial; Dermal bone; Hedgehog; Neural crest; Osteoblast; Osteoblast osteoprogenetor; Osteoblastogenesis; Osterix; Perichondrium; Periosteum; Runx2 cbfa1 osf1 pebp2 A

Indexed keywords

CYCLOPAMINE; PROTEIN PATCHED 1; PROTEIN PATCHED 2; SONIC HEDGEHOG PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; CARTILAGE CELL; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; LIMB DEVELOPMENT; LONG BONE; NONHUMAN; OSSIFICATION; OSTEOBLAST; PERICHONDRIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SKULL DEVELOPMENT; ZEBRA FISH;

ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CHONDROCYTES; COLLAGEN TYPE X; DOWN-REGULATION; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; OSTEOBLASTS; OSTEOGENESIS; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; VERATRUM ALKALOIDS; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO; ERINACEIDAE; TETRAPODA; VERTEBRATA;

EID: 79751526325     PISSN: 09254773     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mod.2010.11.006     Document Type: Article

References (45)

1. Abzhanov A., Rodda S.J., McMahon A.P., Tabin C.J. Regulation of skeletogenic differentiation in cranial dermal bone. Development 2007, 134:3133-3144.
2. Agren M., Kogerman P., Kleman M.I., Wessling M., Toftgard R. Expression of the PTCH1 tumor suppressor gene is regulated by alternative promoters and a single functional Gli-binding site. Gene 2004, 330:101-114.
3. Arai F., Ohneda O., Miyamoto T., Zhang X.Q., Suda T. Mesenchymal stem cells in perichondrium express activated leukocyte cell adhesion molecule and participate in bone marrow formation. J. Exp. Med. 2002, 195:1549-1563.
4. Avaron F., Hoffman L., Guay D., Akimenko M.A. Characterization of two new zebrafish members of the hedgehog family: atypical expression of a zebrafish indian hedgehog gene in skeletal elements of both endochondral and dermal origins. Dev. Dyn. 2006, 235:478-489.
5. Beresford W.A. Chondroid Bone, Secondary Cartilage, and Metaplasia 1981, Urban & Schwarzenberg, Baltimore, Md, p. xvii, 454 p.
6. Beresford W.A. Cranial skeletal tissues: diversity and evolutionary trends. The Skull 1993, vol. 3:69-130. University of Chicago Press, Chicago. J. Hanken, B.K. Hall (Eds.).
7. Clement A., Wiweger M., von der Hardt S., Rusch M.A., Selleck S.B., Chien C.B., Roehl H.H. Regulation of zebrafish skeletogenesis by ext2/dackel and papst1/pinscher. PLoS Genet. 2008, 4:e1000136.
8. Colnot C. Skeletal cell fate decisions within periosteum and bone marrow during bone regeneration. J. Bone Miner. Res. 2009, 24:274-282.
9. Cubbage C.C., Mabee P.M. Development of the cranium and paired fins in the zebrafish Danio rerio (Ostariophysi, Cyprinidae). J. Morphol. 1996, 229:121-160.
10. De Bari C., Dell'Accio F., Vanlauwe J., Eyckmans J., Khan I.M., Archer C.W., Jones E.A., McGonagle D., Mitsiadis T.A., Pitzalis C., Luyten F.P. Mesenchymal multipotency of adult human periosteal cells demonstrated by single-cell lineage analysis. Arthritis Rheum. 2006, 54:1209-1221.
11. DeLaurier A., Eames B.F., Blanco-Sanchez B., Peng G., He X., Swartz M.E., Ullmann B., Westerfield M., Kimmel C.B. Zebrafish sp7:EGFP: a transgenic for studying otic vesicle formation, skeletogenesis, and bone regeneration. Genesis 2010, 48:505-511.
12. Eames B.F., Singer A., Smith G.A., Wood Z.A., Yan Y.L., He X., Polizzi S.J., Catchen J.M., Rodriguez-Mari A., Linbo T., Raible D.W., Postlethwait J.H. UDP xylose synthase 1 is required for morphogenesis and histogenesis of the craniofacial skeleton. Dev. Biol. 2010, 341:400-415.
13. Fisher S., Jagadeeswaran P., Halpern M.E. Radiographic analysis of zebrafish skeletal defects. Dev. Biol. 2003, 264:64-76.
14. Flores M.V., Lam E.Y., Crosier P., Crosier K. A hierarchy of Runx transcription factors modulate the onset of chondrogenesis in craniofacial endochondral bones in zebrafish. Dev. Dyn. 2006, 235:3166-3176.
15. Flores M.V., Tsang V.W., Hu W., Kalev-Zylinska M., Postlethwait J., Crosier P., Crosier K., Fisher S. Duplicate zebrafish runx2 orthologues are expressed in developing skeletal elements. Gene Expr. Patterns 2004, 4:573-581.
16. Gao B., Guo J., She C., Shu A., Yang M., Tan Z., Yang X., Guo S., Feng G., He L. Mutations in IHH, encoding Indian hedgehog, cause brachydactyly type A-1. Nat. Genet. 2001, 28:386-388.
17. Gerstenfeld L.C., Shapiro F.D. Expression of bone-specific genes by hypertrophic chondrocytes: implication of the complex functions of the hypertrophic chondrocyte during endochondral bone development. J. Cell Biochem. 1996, 62:1-9.
18. Hammond C.L., Schulte-Merker S. Two populations of endochondral osteoblasts with differential sensitivity to Hedgehog signalling. Development 2009, 136:3991-4000.
19. Hellemans J., Coucke P.J., Giedion A., De Paepe A., Kramer P., Beemer F., Mortier G.R. Homozygous mutations in IHH cause acrocapitofemoral dysplasia, an autosomal recessive disorder with cone-shaped epiphyses in hands and hips. Am. J. Hum. Genet. 2003, 72:1040-1046.
20. Huysseune A. Skeletal system/microscopic functional anatomy. Handbook of Experimental Animals 2000, 307-317. Academic Press, New York. G. Ostrander (Ed.).
21. Ingham P.W., McMahon A.P. Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 2001, 15:3059-3087.
22. Karlsson C., Thornemo M., Henriksson H.B., Lindahl A. Identification of a stem cell niche in the zone of Ranvier within the knee joint. J. Anat. 2009, 215:355-363.
23. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., Schilling T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 1995, 203:253-310.
24. Koudijs M.J., den Broeder M.J., Keijser A., Wienholds E., Houwing S., van Rooijen E.M., Geisler R., van Eeden F.J. The zebrafish mutants dre, uki, and lep encode negative regulators of the hedgehog signaling pathway. PLoS Genet. 2005, 1:e19.
25. Kronenberg H.M. The role of the perichondrium in fetal bone development. Ann. NY Acad. Sci. 2007, 1116:59-64.
26. Lang M.R., Lapierre L.A., Frotscher M., Goldenring J.R., Knapik E.W. Secretory COPII coat component Sec23a is essential for craniofacial chondrocyte maturation. Nat. Genet. 2006, 38:1198-1203.
27. Li N., Felber K., Elks P., Croucher P., Roehl H.H. Tracking gene expression during zebrafish osteoblast differentiation. Dev. Dyn. 2009, 238:459-466.
28. Long F., Chung U.I., Ohba S., McMahon J., Kronenberg H.M., McMahon A.P. Ihh signaling is directly required for the osteoblast lineage in the endochondral skeleton. Development 2004, 131:1309-1318.
29. Nakashima K., Zhou X., Kunkel G., Zhang Z., Deng J.M., Behringer R.R., de Crombrugghe B. The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell 2002, 108:17-29.
30. Olsen B.R., Reginato A.M., Wang W. Bone development. Annu. Rev. Cell Dev. Biol. 2000, 16:191-220.
31. Roehl H.H., Pacifici M. Shop talk: sugars, bones, and a disease called multiple hereditary exostoses. Dev. Dyn. 2010, 239:1901-1904.
32. Schilling T.F., Kimmel C.B. Segment and cell type lineage restrictions during pharyngeal arch development in the zebrafish embryo. Development 1994, 120:483-494.
33. Schwend T., Ahlgren S.C. Zebrafish con/disp1 reveals multiple spatiotemporal requirements for Hedgehog-signaling in craniofacial development. BMC Dev. Biol. 2009, 9:59.
34. Shapiro F., Holtrop M.E., Glimcher M.J. Organization and cellular biology of the perichondrial ossification groove of ranvier: a morphological study in rabbits. J. Bone Joint Surg. Am. 1977, 59:703-723.
35. Shimoyama A., Wada M., Ikeda F., Hata K., Matsubara T., Nifuji A., Noda M., Amano K., Yamaguchi A., Nishimura R., Yoneda T. Ihh/Gli2 signaling promotes osteoblast differentiation by regulating Runx2 expression and function. Mol. Biol. Cell 2007, 18:2411-2418.
36. St-Jacques B., Hammerschmidt M., McMahon A.P. Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev. 1999, 13:2072-2086.
37. Thisse C., Thisse B. High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat. Protoc. 2008, 3:59-69.
38. van der Meulen T., Kranenbarg S., Schipper H., Samallo J., van Leeuwen J.L., Franssen H. Identification and characterisation of two runx2 homologues in zebrafish with different expression patterns. Biochim. Biophys. Acta 2005, 1729:105-117.
39. Verreijdt L., Debiais-Thibaud M., Borday-Birraux V., Van der Heyden C., Sire J.Y., Huysseune A. Expression of the dlx gene family during formation of the cranial bones in the zebrafish (Danio rerio): differential involvement in the visceral skeleton and braincase. Dev. Dyn. 2006, 235:1371-1389.
40. Vortkamp A., Lee K., Lanske B., Segre G.V., Kronenberg H.M., Tabin C.J. Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 1996, 273:613-622.
41. Wada N., Javidan Y., Nelson S., Carney T.J., Kelsh R.N., Schilling T.F. Hedgehog signaling is required for cranial neural crest morphogenesis and chondrogenesis at the midline in the zebrafish skull. Development 2005, 132:3977-3988.
42. Westerfield, M., 2000. The zebrafish book. A guide for the laboratory use of zebrafish (Danio rerio). University of Oregon Press, Eugene.
43. Witten P.E., Huysseune A. A comparative view on mechanisms and functions of skeletal remodelling in teleost fish, with special emphasis on osteoclasts and their function. Biol. Rev. Camb. Philos. Soc. 2009, 84:315-346.
44. Wolff C., Roy S., Ingham P.W. Multiple muscle cell identities induced by distinct levels and timing of hedgehog activity in the zebrafish embryo. Curr. Biol. 2003, 13:1169-1181.
45. Yan Y.L., Miller C.T., Nissen R.M., Singer A., Liu D., Kirn A., Draper B., Willoughby J., Morcos P.A., Amsterdam A., Chung B.C., Westerfield M., Haffter P., Hopkins N., Kimmel C., Postlethwait J.H. A zebrafish sox9 gene required for cartilage morphogenesis. Development 2002, 129:5065-5079.