Raymond Teck Ho Lee1, Ela W. Knapik2, Jean Paul Thiery1,3,4 and Thomas J. Carney1
1 - Institute of Molecular and Cell Biology (IMCB), Agency for Science, Technology and Research (A*STAR), 61 Biopolis Drive, Singapore 138673, Republic of Singapore
2 - Department of Medicine, Division of Genetic Medicine, Vanderbilt University Medical Center, Nashville, Tennessee 37232, USA
3 - Department of Biochemistry, Yong Loo Lin School of Medicine, National University of Singapore, 117597, Singapore
4 - Cancer Science Institute, National University of Singapore, 117599, Singapore
Published in Development 140(14) 201; doi:10.1242/dev.093534
The neural crest is a multipotent stem cell population that arises from the dorsal aspect of the neural tube and generates both non-ectomesenchymal (melanocytes, peripheral neurons and glia) and ectomesenchymal (skeletogenic, odontogenic, cartilaginous and connective tissue) derivatives. In amniotes, only cranial neural crest generates both classes, with trunk neural crest restricted to nonectomesenchyme. By contrast, it has been suggested that anamniotes might generate derivatives of both classes at all axial levels, with trunk neural crest generating fin osteoblasts, scale mineral-forming cells and connective tissue cells; however, this has not been fully tested. The cause and evolutionary significance of this cranial/trunk dichotomy, and its absence in anamniotes, are debated. Recent experiments have disputed the contribution of fish trunk neural crest to fin osteoblasts and scale mineral-forming cells. This prompted us to test the contribution of anamniote trunk neural crest to fin connective tissue cells. Using genetic-based lineage tracing in zebrafish, we find that these fin mesenchyme cells derive entirely from the mesoderm and that neural crest makes no contribution. Furthermore, contrary to previous suggestions, larval fin mesenchyme cells do not generate the skeletogenic cells of the adult fin, but persist to form fibroblasts associated with adult fin rays. Our data demonstrate that zebrafish trunk neural crest does not generate ectomesenchymal derivatives and challenge long-held ideas about trunk neural crest fate. These findings have important implications for the ontogeny and evolution of the neural crest.
Figure Legend: All fin mesenchyme cells derive from paraxial mesoderm. (A) Confocal image of the tail region of a 48-hpf ntla:gal4; uas:kaede embryo.(B-B”) Immunofluorescent staining of 48-hpf ntla:gal4; uas:kaede; ET37 triple transgenic embryo showing total overlap (B”) of Kaede signal (red, B,B”) and eGFP (green, B’,B”) in the fin. (C-E’) Fluorescent images alone (C,D,E) and superimposed on Nomarski images (C’,D’,E’) of the trunk/tail of 48hpf embryos. The myotome (C,C’), sclerotome (D,D’) and dermomyotome (E,E’) are labelled by actc1b:Gal4i269; uas:kaede (C,C’), Ola-Twist:Gal4; uas:kaede (D,D’) and TgBAC(pax3a:EGFP)i150 (E,E’) transgenics, respectively. (F) Stills taken from time-lapse Movie 4 (see supplementary material Movie 4) of the tail region of a TgBAC(pax3a:EGFP)i150 embryo at 24 hpf (left panel) with subsequent time points at given intervals (in minutes) in the panels to the right. Two fin mesenchyme cells can be tracked (arrows) from the dermomyotome into the fins. Note that eGFP expression is higher in neural crest and dorsal neural tube than in dermomyotome.
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