Home LiteratureArticle Details
PMID: 23213474 Published · ppublish English Journal Article

Fss/Tbx6 is required for central dermomyotome cell fate in zebrafish.

Biology open ·Vol. 1 ·No. 8 ·2012-08-15 ·Pages 806-14

Windner SE, Bird NC, Patterson SE, Doris RA, Devoto SH

Abstract

The dermomyotome is a pool of progenitor cells on the surface of the myotome. In zebrafish, dermomyotome precursors (anterior border cells, ABCs) can be first identified in the anterior portion of recently formed somites. They must be prevented from undergoing terminal differentiation during segmentation, even while mesodermal cells around them respond to signaling cues and differentiate.T-box containing transcription factors regulate many aspects of mesoderm fate including segmentation and somite patterning. The fused somites (fss) gene is the zebrafish ortholog of tbx6. We demonstrate that in addition to its requirement for segmentation, fss/tbx6 is also required for the specification of ABCs and subsequently the central dermomyotome. The absence of Tbx6-dependent central dermomyotome cells in fss/tbx6 mutants is spatially coincident with a patterning defect in the myotome.Using transgenic fish with a heat-shock inducible tbx6 gene in the fss/tbx6 mutant background, we further demonstrate that ubiquitous fss/tbx6 expression has spatially distinct effects on recovery of the dermomyotome and segment boundaries, suggesting that the mechanism of Fss/Tbx6 action is distinct with respect to dermomyotome development and segmentation.We propose that Fss/Tbx6 is required for preventing myogenic differentiation of central dermomyotome precursors before and after segmentation and that central dermomyotome cells represent a genetically and functionally distinct subpopulation within the zebrafish dermomyotome.

Keywords
Anterior Border Cells Fast muscle Muscle pioneer Myogenesis Segmentation Slow muscle Somite
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Windner Stefanie Elisabeth
Department of Biology, Wesleyan University , Middletown, CT 06459 , USA ; Division of Zoology and Functional Anatomy, Department of Organismic Biology, University of Salzburg , A-5020 Salzburg, Austria.
Bird Nathan Craig
Patterson Sara Elizabeth
Doris Rosemarie Anne
Devoto Stephen Henri
References (56)
56 references, click to expand
  1. Clustal W and Clustal X version 2.0.
    Bioinformatics. 2007 Nov 1;23(21):2947-8 PMID: 17846036
  2. Expression of the oscillating gene her1 is directly regulated by Hairy/Enhancer of Split, T-box, and Suppressor of Hairless proteins in the zebrafish segmentation clock.
    Dev Dyn. 2009 Nov;238(11):2745-59 PMID: 19795510
  3. Nodal activity around Kupffer's vesicle depends on the T-box transcription factors Notail and Spadetail and on Notch signaling.
    Dev Dyn. 2007 Aug;236(8):2131-46 PMID: 17654709
  4. Developmental regulation of zebrafish MyoD in wild-type, no tail and spadetail embryos.
    Development. 1996 Jan;122(1):271-80 PMID: 8565839
  5. The T-box transcription factor Tbx18 maintains the separation of anterior and posterior somite compartments.
    Genes Dev. 2004 May 15;18(10):1209-21 PMID: 15155583
  6. The bHLH regulator pMesogenin1 is required for maturation and segmentation of paraxial mesoderm.
    Genes Dev. 2000 Dec 15;14(24):3204-14 PMID: 11124811
  7. The teleost dermomyotome.
    Dev Dyn. 2007 Sep;236(9):2432-43 PMID: 17654604
  8. SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building.
    Mol Biol Evol. 2010 Feb;27(2):221-4 PMID: 19854763
  9. Coordinate embryonic expression of three zebrafish engrailed genes.
    Development. 1992 Dec;116(4):1001-10 PMID: 1363539
  10. Mutations affecting somite formation and patterning in the zebrafish, Danio rerio.
    Development. 1996 Dec;123:153-64 PMID: 9007237
  11. Three zebrafish MEF2 genes delineate somitic and cardiac muscle development in wild-type and mutant embryos.
    Mech Dev. 1996 Oct;59(2):205-18 PMID: 8951797
  12. Tbx24, encoding a T-box protein, is mutated in the zebrafish somite-segmentation mutant fused somites.
    Nat Genet. 2002 Jun;31(2):195-9 PMID: 12021786
  13. Sdf1a patterns zebrafish melanophores and links the somite and melanophore pattern defects in choker mutants.
    Development. 2007 Mar;134(5):1011-22 PMID: 17267445
  14. Whole-somite rotation generates muscle progenitor cell compartments in the developing zebrafish embryo.
    Dev Cell. 2007 Feb;12(2):207-19 PMID: 17276339
  15. The genetics and embryology of zebrafish metamerism.
    Dev Dyn. 2007 Jun;236(6):1422-49 PMID: 17486630
  16. Location and growth of epaxial myotome precursor cells.
    Development. 1997 Apr;124(8):1601-10 PMID: 9108376
  17. Diversity of expression of engrailed-like antigens in zebrafish.
    Development. 1991 Jul;112(3):821-32 PMID: 1682127
  18. Zebrafish Mesp family genes, mesp-a and mesp-b are segmentally expressed in the presomitic mesoderm, and Mesp-b confers the anterior identity to the developing somites.
    Development. 2000 Apr;127(8):1691-702 PMID: 10725245
  19. Lineage analysis of the avian dermomyotome sheet reveals the existence of single cells with both dermal and muscle progenitor fates.
    Development. 2005 Feb;132(4):689-701 PMID: 15659485
  20. tbx6, a Brachyury-related gene expressed by ventral mesendodermal precursors in the zebrafish embryo.
    Dev Biol. 1997 Mar 1;183(1):61-73 PMID: 9119115
  21. Cell-autonomous action of zebrafish spt-1 mutation in specific mesodermal precursors.
    Nature. 1990 Dec 20-27;348(6303):728-30 PMID: 2259382
  22. The fub-1 mutation blocks initial myofibril formation in zebrafish muscle pioneer cells.
    Dev Biol. 1991 Nov;148(1):23-30 PMID: 1936560
  23. Development of the lateral musculature in the teleost, Brachydanio rerio: a fine structural study.
    Am J Anat. 1969 Aug;125(4):457-93 PMID: 5822973
  24. Medial pioneer fibers pattern the morphogenesis of early myoblasts derived from the lateral somite.
    Dev Biol. 2007 May 15;305(2):439-50 PMID: 17382923
  25. Early development of the myotome in the mouse.
    Dev Dyn. 1999 Nov;216(3):219-32 PMID: 10590474
  26. Generality of vertebrate developmental patterns: evidence for a dermomyotome in fish.
    Evol Dev. 2006 Jan-Feb;8(1):101-10 PMID: 16409387
  27. Laser-induced gene expression in specific cells of transgenic zebrafish.
    Development. 2000 May;127(9):1953-60 PMID: 10751183
  28. Examining pattern formation in mouse, chicken and frog embryos with an En-specific antiserum.
    Development. 1991 Feb;111(2):287-98 PMID: 1680044
  29. Multiple muscle cell identities induced by distinct levels and timing of hedgehog activity in the zebrafish embryo.
    Curr Biol. 2003 Jul 15;13(14):1169-81 PMID: 12867027
  30. Fgf8 drives myogenic progression of a novel lateral fast muscle fibre population in zebrafish.
    Development. 2005 Oct;132(19):4211-22 PMID: 16120642
  31. How is myogenesis initiated in the embryo?
    Trends Genet. 1996 Jun;12(6):218-23 PMID: 8928226
  32. A common somitic origin for embryonic muscle progenitors and satellite cells.
    Nature. 2005 Jun 16;435(7044):954-8 PMID: 15843802
  33. Expression patterns of engrailed-like proteins in the chick embryo.
    Dev Dyn. 1992 Apr;193(4):370-88 PMID: 1354990
  34. Zebrafish slow muscle cell migration induces a wave of fast muscle morphogenesis.
    Dev Cell. 2004 Dec;7(6):917-23 PMID: 15572133
  35. Distinct and dynamic myogenic populations in the vertebrate embryo.
    Curr Opin Genet Dev. 2009 Oct;19(5):444-53 PMID: 19762225
  36. Defective somite patterning in mouse embryos with reduced levels of Tbx6.
    Development. 2003 Apr;130(8):1681-90 PMID: 12620991
  37. Tbx6, a mouse T-Box gene implicated in paraxial mesoderm formation at gastrulation.
    Dev Biol. 1996 Dec 15;180(2):534-42 PMID: 8954725
  38. Distinct mechanisms regulate slow-muscle development.
    Curr Biol. 2001 Sep 18;11(18):1432-8 PMID: 11566102
  39. Molecular basis of cell migration in the fish lateral line: role of the chemokine receptor CXCR4 and of its ligand, SDF1.
    Proc Natl Acad Sci U S A. 2002 Dec 10;99(25):16297-302 PMID: 12444253
  40. Three neural tubes in mouse embryos with mutations in the T-box gene Tbx6.
    Nature. 1998 Feb 12;391(6668):695-7 PMID: 9490412
  41. Hedgehog acts directly on the zebrafish dermomyotome to promote myogenic differentiation.
    Dev Biol. 2006 Dec 15;300(2):736-46 PMID: 17046741
  42. Patterning embryos with oscillations: structure, function and dynamics of the vertebrate segmentation clock.
    Development. 2012 Feb;139(4):625-39 PMID: 22274695
  43. Epaxial-adaxial-hypaxial regionalisation of the vertebrate somite: evidence for a somitic organiser and a mirror-image duplication.
    Dev Genes Evol. 2001 Apr;211(4):198-217 PMID: 11455436
  44. T-box genes in early embryogenesis.
    Dev Dyn. 2004 Jan;229(1):201-18 PMID: 14699590
  45. Dynamic somite cell rearrangements lead to distinct waves of myotome growth.
    Development. 2007 Apr;134(7):1253-7 PMID: 17314134
  46. MyoD and Myogenin expression during myogenic phases in brown trout: a precocious onset of mosaic hyperplasia is a prerequisite for fast somatic growth.
    Dev Dyn. 2007 Apr;236(4):1106-14 PMID: 17315228
  47. The zebrafish slow-muscle-omitted gene product is required for Hedgehog signal transduction and the development of slow muscle identity.
    Development. 2000 May;127(10):2189-99 PMID: 10769242
  48. Teasing out T-box targets in early mesoderm.
    Curr Opin Genet Dev. 2008 Oct;18(5):418-25 PMID: 18778771
  49. Interactions between muscle fibers and segment boundaries in zebrafish.
    Dev Biol. 2005 Nov 15;287(2):346-60 PMID: 16225858
  50. Tbx6 regulates left/right patterning in mouse embryos through effects on nodal cilia and perinodal signaling.
    PLoS One. 2008 Jun 25;3(6):e2511 PMID: 18575602
  51. Automated identification of conserved synteny after whole-genome duplication.
    Genome Res. 2009 Aug;19(8):1497-505 PMID: 19465509
  52. Gateway compatible vectors for analysis of gene function in the zebrafish.
    Dev Dyn. 2007 Nov;236(11):3077-87 PMID: 17948311
  53. Phases of myogenic cell activation and possible role of dermomyotome cells in teleost muscle formation.
    Dev Dyn. 2006 Nov;235(11):3132-43 PMID: 16960856
  54. Groucho-associated transcriptional repressor ripply1 is required for proper transition from the presomitic mesoderm to somites.
    Dev Cell. 2005 Dec;9(6):735-44 PMID: 16326386
  55. Integrinalpha5 and delta/notch signaling have complementary spatiotemporal requirements during zebrafish somitogenesis.
    Dev Cell. 2005 Apr;8(4):575-86 PMID: 15809039
  56. Signals and myogenic regulatory factors restrict pax3 and pax7 expression to dermomyotome-like tissue in zebrafish.
    Dev Biol. 2007 Feb 15;302(2):504-21 PMID: 17094960
Article Info
Journal
Biology open
Abbr.
Biol Open
ISSN
2046-6390
Published
2012-08-15
Epub
2012-00-29
Pages
806-14
Language
English
Region
England
NLM ID
101578018
PMCID
PMC3507223
Grants
NICHD NIH HHS · R01 HD037509 · United States
NIAMS NIH HHS · R15 AR066284 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]