A switch from low to high shh activity regulates establishment of limb progenitors and signaling centers

Developmental Cell

Volumn 29, Issue 2, 2014, Pages 241-249

  Zhulyn, Olena ^a,b   Li, Danyi ^a,b   Deimling, Steven ^a   Vakili, Niki Alizadeh ^a,b   Mo, Rong ^a   Puviindran, Vijitha ^a   Chen, Miao Hsueh ^c,d   Chuang, Pao Tien ^c   Hopyan, Sevan ^a,b   Hui, Chi chung ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GLI3; TRANSCRIPTION FACTOR HAND2; TRANSCRIPTION FACTOR KIF7; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHICKEN; CONTROLLED STUDY; EMBRYO; FORELIMB; LIMB; LIMB BUD; LIMB DEVELOPMENT; MOUSE; NONHUMAN; POPULATION MODEL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STEM CELL EXPANSION;

ERINACEIDAE; VERTEBRATA;

ANIMALS; ANIMALS, OUTBRED STRAINS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BODY PATTERNING; CATTLE; CHICKENS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; KINESIN; KRUPPEL-LIKE TRANSCRIPTION FACTORS; LIMB BUDS; MICE; NERVE TISSUE PROTEINS; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION;

EID: 84899656162     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2014.03.002     Document Type: Article

References (34)

1. Ahn S., Joyner A.L. Dynamic changes in the response of cells to positive hedgehog signaling during mouse limb patterning. Cell 2004, 118:505-516.
2. Bai C.B., Auerbach W., Lee J.S., Stephen D., Joyner A.L. Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. Development 2002, 129:4753-4761.
3. Bowers M., Eng L., Lao Z., Turnbull R.K., Bao X., Riedel E., Mackem S., Joyner A.L. Limb anterior-posterior polarity integrates activator and repressor functions of GLI2 as well as GLI3. Dev. Biol. 2012, 370:110-124.
4. Butterfield N.C., Metzis V., McGlinn E., Bruce S.J., Wainwright B.J., Wicking C. Patched 1 is a crucial determinant of asymmetry and digit number in the vertebrate limb. Development 2009, 136:3515-3524.
5. Cao T., Wang C., Yang M., Wu C., Wang B. Mouse limbs expressing only the Gli3 repressor resemble those of Sonic hedgehog mutants. Dev. Biol. 2013, 379:221-228.
6. Chen M.-H., Wilson C.W., Li Y.-J., Law K.K., Lu C.-S., Gacayan R., Zhang X., Hui C.C., Chuang P.-T. Cilium-independent regulation of Gli protein function by Sufu in Hedgehog signaling is evolutionarily conserved. Genes Dev. 2009, 23:1910-1928.
7. Cheung H.O.-L., Zhang X., Ribeiro A., Mo R., Makino S., Puviindran V., Law K.K.L., Briscoe J., Hui C.-C. The kinesin protein Kif7 is a critical regulator of Gli transcription factors in mammalian hedgehog signaling. Sci. Signal. 2009, 2:ra29. 10.1126/scisignal.2000405.
8. Chiang C., Litingtung Y., Harris M.P., Simandl B.K., Li Y., Beachy P.A., Fallon J.F. Manifestation of the limb prepattern: limb development in the absence of sonic hedgehog function. Dev. Biol. 2001, 236:421-435.
9. Ding Q., Motoyama J., Gasca S., Mo R., Sasaki H., Rossant J., Hui C.-C. Diminished Sonic hedgehog signaling and lack of floor plate differentiation in Gli2 mutant mice. Development 1998, 125:2533-2543.
10. Ellis T., Smyth I., Riley E., Graham S., Elliot K., Narang M., Kay G.F., Wicking C., Wainwright B. Patched 1 conditional null allele in mice. Genesis 2003, 36:158-161.
11. Galli A., Robay D., Osterwalder M., Bao X., Bénazet J.-D., Tariq M., Paro R., Mackem S., Zeller R. Distinct roles of Hand2 in initiating polarity and posterior Shh expression during the onset of mouse limb bud development. PLoS Genet. 2010, 6:e1000901.
12. Goodrich L.V., Milenkovic L., Higgins K.M., Scott M.P. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 1997, 277:1109-1113.
13. Harfe B.D., Scherz P.J., Nissim S., Tian H., McMahon A.P., Tabin C.J. Evidence for an expansion-based temporal Shh gradient in specifying vertebrate digit identities. Cell 2004, 118:517-528.
14. Hayashi S., McMahon A.P. Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev. Biol. 2002, 244:305-318.
15. Hill P., Götz K., Rüther U. A SHH-independent regulation of Gli3 is a significant determinant of anteroposterior patterning of the limb bud. Dev. Biol. 2009, 328:506-516.
16. Lewandoski M., Sun X., Martin G.R. Fgf8 signalling from the AER is essential for normal limb development. Nat. Genet. 2000, 26:460-463.
17. Li Z.J., Nieuwenhuis E., Nien W., Zhang X., Zhang J., Puviindran V., Wainwright B.J., Kim P.C.W., Hui C.-C. Kif7 regulates Gli2 through Sufu-dependent and -independent functions during skin development and tumorigenesis. Development 2012, 139:4152-4161.
18. Li D., Sakuma R., Vakili N.A., Mo R., Puviindran V., Deimling S., Zhang X., Hopyan S., Hui C.-c. Formation of proximal and anterior limb skeleton requires early function of Irx3 and Irx5 and is negatively regulated by Shh signaling. Dev. Cell 2014, 29:233-240. this issue.
19. Litingtung Y., Dahn R.D., Li Y., Fallon J.F., Chiang C. Shh and Gli3 are dispensable for limb skeleton formation but regulate digit number and identity. Nature 2002, 418:979-983.
20. Logan M., Martin J.F., Nagy A., Lobe C., Olson E.N., Tabin C.J. Expression of Cre Recombinase in the developing mouse limb bud driven by a Prxl enhancer. Genesis 2002, 33:77-80.
21. Lopez-Rios J., Speziale D., Robay D., Scotti M., Osterwalder M., Nusspaumer G., Galli A., Holländer G.A., Kmita M., Zeller R. GLI3 constrains digit number by controlling both progenitor proliferation and BMP-dependent exit to chondrogenesis. Dev. Cell 2012, 22:837-848.
22. Masuya H., Sagai T., Moriwaki K., Shiroishi T. Multigenic control of the localization of the zone of polarizing activity in limb morphogenesis in the mouse. Dev. Biol. 1997, 182:42-51.
23. Riddle R.D., Johnson R.L., Laufer E., Tabin C. Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 1993, 75:1401-1416.
24. Rohatgi R., Milenkovic L., Scott M.P. Patched1 regulates hedgehog signaling at the primary cilium. Science 2007, 317:372-376.
25. te Welscher P., Fernandez-Teran M., Ros M.A., Zeller R. Mutual genetic antagonism involving GLI3 and dHAND prepatterns the vertebrate limb bud mesenchyme prior to SHH signaling. Genes Dev. 2002, 16:421-426.
26. te Welscher P., Zuniga A., Kuijper S., Drenth T., Goedemans H.J., Meijlink F., Zeller R. Progression of vertebrate limb development through SHH-mediated counteraction of GLI3. Science 2002, 298:827-830.
27. Tickle C., Summerbell D., Wolpert L. Positional signalling and specification of digits in chick limb morphogenesis. Nature 1975, 254:199-202.
28. Towers M., Mahood R., Yin Y., Tickle C. Integration of growth and specification in chick wing digit-patterning. Nature 2008, 452:882-886.
29. Urs S., Harrington A., Liaw L., Small D. Selective expression of an aP2/Fatty Acid Binding Protein 4-Cre transgene in non-adipogenic tissues during embryonic development. Transgenic Res. 2006, 15:647-653.
30. Vokes S.A., Ji H., Wong W.H., McMahon A.P. A genome-scale analysis of the cis-regulatory circuitry underlying sonic hedgehog-mediated patterning of the mammalian limb. Genes Dev. 2008, 22:2651-2663.
31. Wang B., Fallon J.F., Beachy P.A. Hedgehog-regulated processing of Gli3 produces an anterior/posterior repressor gradient in the developing vertebrate limb. Cell 2000, 100:423-434.
32. Wang C., Pan Y., Wang B. Suppressor of fused and Spop regulate the stability, processing and function of Gli2 and Gli3 full-length activators but not their repressors. Development 2010, 137:2001-2009.
33. Zhu J., Nakamura E., Nguyen M.-T., Bao X., Akiyama H., Mackem S. Uncoupling Sonic hedgehog control of pattern and expansion of the developing limb bud. Dev. Cell 2008, 14:624-632.
34. Zhulyn O., Hui C. GLI Proteins in Human Genetic Disease. eLS 2012, Published online December 17, 2012. 10.1002/9780470015902.a0024402.