Bone regenerates via dedifferentiation of osteoblasts in the zebrafish fin

Developmental Cell

Volumn 20, Issue 5, 2011, Pages 713-724

  Knopf, Franziska ^a   Hammond, Christina ^b,d   Chekuru, Avinash ^a   Kurth, Thomas ^a   Hans, Stefan ^a   Weber, Christopher W ^c   Mahatma, Gina ^c   Fisher, Shannon ^c   Brand, Michael ^a   Schulte Merker, Stefan ^b   Weidinger, Gilbert ^a  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b HUBRECHT INSTITUTE   (Netherlands)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMICAL MARKER;

ANIMAL CELL; ARTICLE; BLASTEMA; BONE REGENERATION; BONE REMODELING; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; DOWN REGULATION; FIN (ORGAN); GENE EXPRESSION; MULTIPOTENT STEM CELL; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; ZEBRA FISH;

ANIMAL FINS; ANIMALS; BONE AND BONES; CELL DEDIFFERENTIATION; DOWN-REGULATION; OSTEOBLASTS; ZEBRAFISH;

DANIO RERIO; MAMMALIA;

EID: 79955926225     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2011.04.014     Document Type: Article

References (52)

1. Alford A.I., Hankenson K.D. Matricellular proteins: extracellular modulators of bone development, remodeling, and regeneration. Bone 2006, 38:749-757.
2. Brockes J.P., Kumar A. Plasticity and reprogramming of differentiated cells in amphibian regeneration. Nat. Rev. Mol. Cell Biol. 2002, 3:566-574.
3. Brockes J.P., Kumar A. Appendage regeneration in adult vertebrates and implications for regenerative medicine. Science 2005, 310:1919-1923.
4. Colnot C. Skeletal cell fate decisions within periosteum and bone marrow during bone regeneration. J. Bone Miner. Res. 2009, 24:274-282.
5. Echeverri K., Clarke J.D., Tanaka E.M. In vivo imaging indicates muscle fiber dedifferentiation is a major contributor to the regenerating tail blastema. Dev. Biol. 2001, 236:151-164.
6. Fisher S., Grice E.A., Vinton R.M., Bessling S.L., McCallion A.S. Conservation of RET regulatory function from human to zebrafish without sequence similarity. Science 2006, 312:276-279.
7. Fisher S., Grice E.A., Vinton R.M., Bessling S.L., Urasaki A., Kawakami K., McCallion A.S. Evaluating the biological relevance of putative enhancers using Tol2 transposon-mediated transgenesis in zebrafish. Nat. Protoc. 2006, 1:1297-1305.
8. Gavaia P.J., Simes D.C., Ortiz-Delgado J.B., Viegas C.S., Pinto J.P., Kelsh R.N., Sarasquete M.C., Cancela M.L. Osteocalcin and matrix Gla protein in zebrafish (Danio rerio) and Senegal sole (Solea senegalensis): comparative gene and protein expression during larval development through adulthood. Gene Expr. Patterns 2006, 6:637-652.
9. Goss R.J., Stagg M.W. The regeneration of fins and fin rays in Fundulus heteroclitus. J. Exp. Zool. 1957, 136:487-507.
10. Grabher C., Joly J.S., Wittbrodt J. Highly efficient zebrafish transgenesis mediated by the meganuclease I-SceI. Methods Cell Biol. 2004, 77:381-401.
11. Hall B.K. Bones and Cartilage: Developmental and Evolutionary Skeletal Biology 2005, Volume 1. Elsevier Academic Press, San Diego, CA.
12. Halloran M.C., Sato-Maeda M., Warren J.T., Su F., Lele Z., Krone P.H., Kuwada J.Y., Shoji W. Laser-induced gene expression in specific cells of transgenic zebrafish. Development 2000, 127:1953-1960.
13. Han M., Yang X., Taylor G., Burdsal C.A., Anderson R.A., Muneoka K. Limb regeneration in higher vertebrates: developing a roadmap. Anat. Rec. B New Anat. 2005, 287:14-24.
14. Hans S., Kaslin J., Freudenreich D., Brand M. Temporally-controlled site-specific recombination in zebrafish. PLoS One 2009, 4:e4640.
15. Inohaya K., Takano Y., Kudo A. The teleost intervertebral region acts as a growth center of the centrum: in vivo visualization of osteoblasts and their progenitors in transgenic fish. Dev. Dyn. 2007, 236:3031-3046.
16. Jazwinska A., Badakov R., Keating M.T. Activin-ßA signaling is required for zebrafish fin regeneration. Curr. Biol. 2007, 17:1390-1395.
17. Johnson S.L., Weston J.A. Temperature-sensitive mutations that cause stage-specific defects in zebrafish fin regeneration. Genetics 1995, 141:1583-1595.
18. Johnson S.L., Bennett P. Growth control in the ontogenetic and regenerating zebrafish fin. Methods Cell Biol. 1999, 59:301-311.
19. Jopling C., Sleep E., Raya M., Marti M., Raya A., Belmonte J.C. Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature 2010, 464:606-609.
20. Kikuchi K., Holdway J.E., Werdich A.A., Anderson R.M., Fang Y., Egnaczyk G.F., Evans T., Macrae C.A., Stainier D.Y., Poss K.D. Primary contribution to zebrafish heart regeneration by gata4(+) cardiomyocytes. Nature 2010, 464:601-605.
21. Komori T., Yagi H., Nomura S., Yamaguchi A., Sasaki K., Deguchi K., Shimizu Y., Bronson R.T., Gao Y.H., Inada M., et al. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 1997, 89:755-764.
22. Kragl M., Knapp D., Nacu E., Khattak S., Maden M., Epperlein H.H., Tanaka E.M. Cells keep a memory of their tissue origin during axolotl limb regeneration. Nature 2009, 460:60-65.
23. Li N., Felber K., Elks P., Croucher P., Roehl H.H. Tracking gene expression during zebrafish osteoblast differentiation. Dev. Dyn. 2009, 238:459-466.
24. Lo D.C., Allen F., Brockes J.P. Reversal of muscle differentiation during urodele limb regeneration. Proc. Natl. Acad. Sci. USA 1993, 90:7230-7234.
25. Mackie E.J., Tucker R.P. Tenascin in bone morphogenesis: expression by osteoblasts and cell type-specific expression of splice variants. J. Cell Sci. 1992, 103:765-771.
26. Maes C., Kobayashi T., Selig M.K., Torrekens S., Roth S.I., Mackem S., Carmeliet G., Kronenberg H.M. Osteoblast precursors, but not mature osteoblasts, move into developing and fractured bones along with invading blood vessels. Dev. Cell 2010, 19:329-344.
27. Marí-Beffa M., Santamaria J.A., Murciano C., Santos-Ruiz L., Andrades J.A., Guerado E., Becerra J. Zebrafish fins as a model system for skeletal human studies. ScientificWorldJournal 2007, 7:1114-1127.
28. Metzger D., Clifford J., Chiba H., Chambon P. Conditional site-specific recombination in mammalian cells using a ligand-dependent chimeric Cre recombinase. Proc. Natl. Acad. Sci. USA 1995, 92:6991-6995.
29. Morrison S.J., Kimble J. Asymmetric and symmetric stem-cell divisions in development and cancer. Nature 2006, 441:1068-1074.
30. 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.
31. Nakatani Y., Kawakami Y., Kudo A. Cellular and molecular processes of regeneration, with special emphasis on fish fins. Dev. Growth Differ. 2007, 49:145-154.
32. Nechiporuk A., Keating M.T. A proliferation gradient between proximal and msxb-expressing distal blastema directs zebrafish fin regeneration. Development 2002, 129:2607-2617.
33. Office of the Surgeon General (US). (2003). Report of the Surgeon General's Workshop on Osteoporosis and Bone Health: December 12-13, 2002, Washington, DC. (Rockville, MD: Office of the Surgeon General). http://www.surgeongeneral.gov/topics/bonehealth/workshop_report/workshop_rpt.htm.
34. Pauls S., Geldmacher-Voss B., Campos-Ortega J.A. A zebrafish histone variant H2A.F/Z and a transgenic H2A.F/Z:GFP fusion protein for in vivo studies of embryonic development. Dev. Genes Evol. 2001, 211:603-610.
35. Picker A., Scholpp S., Bohli H., Takeda H., Brand M. A novel positive transcriptional feedback loop in midbrain-hindbrain boundary development is revealed through analysis of the zebrafish pax2.1 promoter in transgenic lines. Development 2002, 129:3227-3239.
36. Pietsch P., Webber R.H. Innervation and regeneration in orbitally transplanted limbs of Amblystoma larvae. Anat. Rec. 1965, 152:439-450.
37. Poleo G., Brown C.W., Laforest L., Akimenko M.-A. Cell proliferation and movement during early fin regeneration in zebrafish. Dev. Dyn. 2001, 221:380-390.
38. Poss K.D. Advances in understanding tissue regenerative capacity and mechanisms in animals. Nat. Rev. Genet. 2010, 11:710-722.
39. Poss K.D., Shen J., Keating M.T. Induction of lef1 during zebrafish fin regeneration. Dev. Dyn. 2000, 219:282-286.
40. Poss K.D., Keating M.T., Nechiporuk A. Tales of regeneration in zebrafish. Dev. Dyn. 2003, 226:202-210.
41. Poss K.D., Shen J., Nechiporuk A., McMahon G., Thisse B., Thisse C., Keating M.T. Roles for Fgf signaling during zebrafish fin regeneration. Dev. Biol. 2000, 222:347-358.
42. Provost E., Rhee J., Leach S.D. Viral 2A peptides allow expression of multiple proteins from a single ORF in transgenic zebrafish embryos. Genesis 2007, 45:625-629.
43. Santos-Ruiz L., Santamaria J.A., Ruiz-Sanchez J., Becerra J. Cell proliferation during blastema formation in the regenerating teleost fin. Dev. Dyn. 2002, 223:262-272.
44. Shaner N.C., Campbell R.E., Steinbach P.A., Giepmans B.N., Palmer A.E., Tsien R.Y. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 2004, 22:1567-1572.
45. Slack J.M. Amphibian muscle regeneration-dedifferentiation or satellite cells?. Trends Cell Biol. 2006, 16:273-275.
46. Slack J.M., Beck C.W., Gargioli C., Christen B. Cellular and molecular mechanisms of regeneration in Xenopus. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2004, 359:745-751.
47. Spoorendonk K.M., Peterson-Maduro J., Renn J., Trowe T., Kranenbarg S., Winkler C., Schulte-Merker S. Retinoic acid and Cyp26b1 are critical regulators of osteogenesis in the axial skeleton. Development 2008, 135:3765-3774.
48. Stocum D.L. The urodele limb regeneration blastema: a self-organizing system. I. Morphogenesis and differentiation of autografted whole and fractional blastemas. Dev. Biol. 1968, 18:457-480.
49. Stoick-Cooper C.L., Moon R.T., Weidinger G. Advances in signaling in vertebrate regeneration as a prelude to regenerative medicine. Genes Dev. 2007, 21:1292-1315.
50. Tanaka E.M. Cell differentiation and cell fate during urodele tail and limb regeneration. Curr. Opin. Genet. Dev. 2003, 13:497-501.
51. Whitehead G.G., Makino S., Lien C.-L., Keating M.T. fgf20 is essential for initiating zebrafish fin regeneration. Science 2005, 310:1957-1960.
52. Wills A.A., Kidd A.R., Lepilina A., Poss K.D. Fgfs control homeostatic regeneration in adult zebrafish fins. Development 2008, 135:3063-3070.