Sonic hedgehog-expressing cells in the developing limb measure time by an intrinsic cell cycle clock

Nature Communications

Volumn 5, Issue , 2014, Pages

  Chinnaiya, Kavitha ^a   Tickle, Cheryll ^b   Towers, Matthew ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b University of Bath   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

RETINOIC ACID; SONIC HEDGEHOG PROTEIN;

CYTOLOGY; DEVELOPMENTAL BIOLOGY; EMBRYO; GENE EXPRESSION; LIMB;

ANTERIOR POSTERIOR AXIS; ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL PROLIFERATION; CELL RENEWAL; DNA CONTENT; EMBRYO; LIMB BUD; LIMB DEVELOPMENT; LIMB REGENERATION; NONHUMAN; POLARIZATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; BIOLOGICAL RHYTHM; CELL CYCLE; CHICK EMBRYO; EMBRYO DEVELOPMENT; EMBRYOLOGY; GENE EXPRESSION REGULATION; LIMB; METABOLISM;

ANIMALS; BIOLOGICAL CLOCKS; CELL CYCLE; CHICK EMBRYO; EMBRYONIC DEVELOPMENT; EXTREMITIES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; TRETINOIN;

EID: 84903977524     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5230     Document Type: Article

References (28)

1. Primmett, D. R., Norris, W. E., Carlson, G. J., Keynes, R. J. & Stern, C. D. Periodic segmental anomalies induced by heat shock in the chick embryo are associated with the cell cycle. Development 105, 119-130 (1989). (Pubitemid 19046656)
2. Primmett, D. R., Stern, C. D. & Keynes, R. J. Heat shock causes repeated segmental anomalies in the chick embryo. Development 104, 331-339 (1988). (Pubitemid 18266512)
3. Duboule, D. Temporal colinearity and the phylotypic progression: a basis for the stability of a vertebrate Bauplan and the evolution of morphologies through heterochrony. Development 135-142 (1994).
4. Summerbell, D., Lewis, J. H. & Wolpert, L. Positional information in chick limb morphogenesis. Nature 244, 492-496 (1973).
5. Lewis, J. H. Fate maps and the pattern of cell division: a calculation for the chick wing-bud. J. Embryol. Exp. Morphol. 33, 419-434 (1975).
6. Mercader, N. et al. Opposing RA and FGF signals control proximodistal vertebrate limb development through regulation of Meis genes. Development 127, 3961-3970 (2000).
7. Rosello-Diez, A., Ros, M. A. & Torres, M. Diffusible signals, not autonomous mechanisms, determine the main proximodistal limb subdivision. Science 332, 1086-1088 (2011).
8. Cooper, K. L. et al. Initiation of proximal-distal patterning in the vertebrate limb by signals and growth. Science 332, 1083-1086 (2011).
9. Stratford, T., Horton, C. & Maden, M. Retinoic acid is required for the initiation of outgrowth in the chick limb bud. Curr. Biol. 6, 1124-1133 (1996). (Pubitemid 26368746)
10. Zhao, X. et al. Retinoic acid promotes limb induction through effects on body axis extension but is unnecessary for limb patterning. Curr. Biol. 19, 1050-1057 (2009).
11. Cunningham, T. J. et al. Antagonism between retinoic acid and fibroblast growth factor signaling during limb development. Cell Rep. 3, 1503-1511 (2013).
12. Dudley, A. T., Ros, M. A. & Tabin, C. J. A re-examination of proximodistal patterning during vertebrate limb development. Nature 418, 539-544 (2002). (Pubitemid 34851400)
13. Mariani, F. V., Ahn, C. P. & Martin, G. R. Genetic evidence that FGFs have an instructive role in limb proximal-distal patterning. Nature 453, 401-405 (2008). (Pubitemid 351693123)
14. Galloway, J. L., Delgado, I., Ros, M. A. & Tabin, C. J. A reevaluation of X-irradiation-induced phocomelia and proximodistal limb patterning. Nature 460, 400-404 (2009).
15. Towers, M., Wolpert, L. & Tickle, C. Gradients of signalling in the developing limb. Curr. Opin. Cell Biol. 24, 181-187 (2012).
16. Tickle, C., Summerbell, D. & Wolpert, L. Positional signalling and specification of digits in chick limb morphogenesis. Nature 254, 199-202 (1975).
17. Riddle, R. D., Johnson, R. L., Laufer, E. & Tabin, C. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75, 1401-1416 (1993). (Pubitemid 24021914)
18. Harfe, B. D. et al. Evidence for an expansion-based temporal Shh gradient in specifying vertebrate digit identities. Cell 118, 517-528 (2004). (Pubitemid 39485670)
19. Scherz, P. J., Harfe, B. D., McMahon, A. P. & Tabin, C. J. The limb bud Shh-Fgf feedback loop is terminated by expansion of former ZPA cells. Science 305, 396-399 (2004). (Pubitemid 38938155)
20. Towers, M., Mahood, R., Yin, Y. & Tickle, C. Integration of growth and specification in chick wing digit-patterning. Nature 452, 882-886 (2008). (Pubitemid 351550856)
21. Towers, M., Signolet, J., Sherman, A., Sang, H. & Tickle, C. Insights into bird wing evolution and digit specification from polarizing region fate maps. Nat. Commun. 2, 426 (2011).
22. Sanz-Ezquerro, J. J. & Tickle, C. Autoregulation of Shh expression and Shh induction of cell death suggest a mechanism for modulating polarising activity during chick limb development. Development 127, 4811-4823 (2000).
23. Summerbell, D. Interaction between the proximo-distal and antero-posterior co-ordinates of positional value during the specification of positional information in the early development of the chick limb-bud. J. Embryol. Exp. Morphol. 32, 227-237 (1974).
24. Gao, F. B., Durand, B. & Raff, M. Oligodendrocyte precursor cells count time but not cell divisions before differentiation. Curr. Biol. 7, 152-155 (1997). (Pubitemid 27155625)
25. Durand, B. & Raff, M. A cell-intrinsic timer that operates during oligodendrocyte development. Bioessays 22, 64-71 (2000). (Pubitemid 30057135)
26. Thaller, C. & Eichele, G. Identification and spatial distribution of retinoids in the developing chick limb bud. Nature 327, 625-628 (1987). (Pubitemid 17086898)
27. Mic, F. A., Sirbu, I. O. & Duester, G. Retinoic acid synthesis controlled by Raldh2 is required early for limb bud initiation and then later as a proximodistal signal during apical ectodermal ridge formation. J. Biol. Chem. 279, 26698-26706 (2004). (Pubitemid 38798827)
28. Probst, S. et al. SHH propagates distal limb bud development by enhancing CYP26B1-mediated retinoic acid clearance via AER-FGF signalling. Development 138, 1913-1923 (2011).