publication . Article . 2016

Differential Cellular Responses to Hedgehog Signalling in Vertebrates—What is the Role of Competence?

Clemens Kiecker; Anthony Graham; Malcolm Logan;
Open Access English
  • Published: 01 Dec 2016 Journal: Journal of Developmental Biology, volume 4, issue 4 (eissn: 2221-3759, Copyright policy)
  • Publisher: MDPI
Abstract
A surprisingly small number of signalling pathways generate a plethora of cellular responses ranging from the acquisition of multiple cell fates to proliferation, differentiation, morphogenesis and cell death. These diverse responses may be due to the dose-dependent activities of signalling factors, or to intrinsic differences in the response of cells to a given signal—a phenomenon called differential cellular competence. In this review, we focus on temporal and spatial differences in competence for Hedgehog (HH) signalling, a signalling pathway that is reiteratively employed in embryos and adult organisms. We discuss the upstream signals and mechanisms that may...
Subjects
free text keywords: Review, chick embryo, Drosophila, iroquois, IRX, limb bud, morphogen, mouse, neural tube, proliferation, temporal adaptation, zebrafish, Biology (General), QH301-705.5, biology.organism_classification, biology, Cell, medicine.anatomical_structure, medicine, Hedgehog signaling pathway, Communication, business.industry, business, Morphogenesis, Signalling, Hedgehog, Neuroscience
Funded by
RCUK| Vertebrate Limb Development 2
Project
  • Funder: Research Council UK (RCUK)
  • Project Code: MC_PC_13052
  • Funding stream: MRC
167 references, page 1 of 12

Spemann, H.. Über Correlationen in der Entwicklung des Auges. Verhand. Anat. Ges.. 1901; 15: 61-79

Waddington, C.H.. Organisers and Genes. 1940

Briscoe, J., Small, S.. Morphogen rules: Design principles of gradient-mediated embryo patterning. Development. 2015; 142: 3996-4009 [OpenAIRE] [PubMed] [DOI]

Ingham, P.W., Nakano, Y., Seger, C.. Mechanisms and functions of hedgehog signalling across the metazoa. Nat. Rev. Genet.. 2011; 12: 393-406 [OpenAIRE] [PubMed] [DOI]

Taipale, J., Cooper, M.K., Maiti, T., Beachy, P.A.. Patched acts catalytically to suppress the activity of Smoothened. Nature. 2002; 418: 892-897 [OpenAIRE] [PubMed] [DOI]

Tukachinsky, H., Petrov, K., Watanabe, M., Salic, A.. Mechanism of inhibition of the tumor suppressor Patched by Sonic Hedgehog. Proc. Natl. Acad. Sci. USA. 2016; 113: E5866-E5875 [OpenAIRE] [PubMed] [DOI]

Bijlsma, M.F., Spek, C.A., Zivkovic, D., van de Water, S., Rezaee, F., Peppelenbosch, M.P.. Repression of smoothened by patched-dependent (pro-)vitamin D3 secretion. PLoS Biol.. 2006; 4 [OpenAIRE] [PubMed] [DOI]

Linder, B., Weber, S., Dittmann, K., Adamski, J., Hahn, H., Uhmann, A.. A Functional and Putative Physiological Role of Calcitriol in Patched1/Smoothened Interaction. J. Biol. Chem.. 2015; 290: 19614-19628 [OpenAIRE] [PubMed] [DOI]

Alfaro, A.C., Roberts, B., Kwong, L., Bijlsma, M.F., Roelink, H.. Ptch2 mediates the Shh response in Ptch1-/- cells. Development. 2014; 141: 3331-3339 [OpenAIRE] [PubMed] [DOI]

Lee, C.S., Buttitta, L., Fan, C.M.. Evidence that the WNT-inducible growth arrest-specific gene 1 encodes an antagonist of sonic hedgehog signaling in the somite. Proc. Natl. Acad. Sci. USA. 2001; 98: 11347-11352 [OpenAIRE] [PubMed] [DOI]

Yao, S., Lum, L., Beachy, P.. The ihog cell-surface proteins bind Hedgehog and mediate pathway activation. Cell. 2006; 125: 343-357 [OpenAIRE] [PubMed] [DOI]

Allen, B.L., Tenzen, T., McMahon, A.P.. The Hedgehog-binding proteins Gas1 and Cdo cooperate to positively regulate Shh signaling during mouse development. Genes Dev.. 2007; 21: 1244-1257 [OpenAIRE] [PubMed] [DOI]

Martinelli, D.C., Fan, C.M.. Gas1 extends the range of Hedgehog action by facilitating its signaling. Genes Dev.. 2007; 21: 1231-1243 [OpenAIRE] [PubMed] [DOI]

Tenzen, T., Allen, B.L., Cole, F., Kang, J.S., Krauss, R.S., McMahon, A.P.. The cell surface membrane proteins Cdo and Boc are components and targets of the Hedgehog signaling pathway and feedback network in mice. Dev. Cell. 2006; 10: 647-656 [OpenAIRE] [PubMed] [DOI]

Chuang, P.T., McMahon, A.P.. Vertebrate Hedgehog signalling modulated by induction of a Hedgehog-binding protein. Nature. 1999; 397: 617-621 [OpenAIRE] [PubMed] [DOI]

167 references, page 1 of 12
Abstract
A surprisingly small number of signalling pathways generate a plethora of cellular responses ranging from the acquisition of multiple cell fates to proliferation, differentiation, morphogenesis and cell death. These diverse responses may be due to the dose-dependent activities of signalling factors, or to intrinsic differences in the response of cells to a given signal—a phenomenon called differential cellular competence. In this review, we focus on temporal and spatial differences in competence for Hedgehog (HH) signalling, a signalling pathway that is reiteratively employed in embryos and adult organisms. We discuss the upstream signals and mechanisms that may...
Subjects
free text keywords: Review, chick embryo, Drosophila, iroquois, IRX, limb bud, morphogen, mouse, neural tube, proliferation, temporal adaptation, zebrafish, Biology (General), QH301-705.5, biology.organism_classification, biology, Cell, medicine.anatomical_structure, medicine, Hedgehog signaling pathway, Communication, business.industry, business, Morphogenesis, Signalling, Hedgehog, Neuroscience
Funded by
RCUK| Vertebrate Limb Development 2
Project
  • Funder: Research Council UK (RCUK)
  • Project Code: MC_PC_13052
  • Funding stream: MRC
167 references, page 1 of 12

Spemann, H.. Über Correlationen in der Entwicklung des Auges. Verhand. Anat. Ges.. 1901; 15: 61-79

Waddington, C.H.. Organisers and Genes. 1940

Briscoe, J., Small, S.. Morphogen rules: Design principles of gradient-mediated embryo patterning. Development. 2015; 142: 3996-4009 [OpenAIRE] [PubMed] [DOI]

Ingham, P.W., Nakano, Y., Seger, C.. Mechanisms and functions of hedgehog signalling across the metazoa. Nat. Rev. Genet.. 2011; 12: 393-406 [OpenAIRE] [PubMed] [DOI]

Taipale, J., Cooper, M.K., Maiti, T., Beachy, P.A.. Patched acts catalytically to suppress the activity of Smoothened. Nature. 2002; 418: 892-897 [OpenAIRE] [PubMed] [DOI]

Tukachinsky, H., Petrov, K., Watanabe, M., Salic, A.. Mechanism of inhibition of the tumor suppressor Patched by Sonic Hedgehog. Proc. Natl. Acad. Sci. USA. 2016; 113: E5866-E5875 [OpenAIRE] [PubMed] [DOI]

Bijlsma, M.F., Spek, C.A., Zivkovic, D., van de Water, S., Rezaee, F., Peppelenbosch, M.P.. Repression of smoothened by patched-dependent (pro-)vitamin D3 secretion. PLoS Biol.. 2006; 4 [OpenAIRE] [PubMed] [DOI]

Linder, B., Weber, S., Dittmann, K., Adamski, J., Hahn, H., Uhmann, A.. A Functional and Putative Physiological Role of Calcitriol in Patched1/Smoothened Interaction. J. Biol. Chem.. 2015; 290: 19614-19628 [OpenAIRE] [PubMed] [DOI]

Alfaro, A.C., Roberts, B., Kwong, L., Bijlsma, M.F., Roelink, H.. Ptch2 mediates the Shh response in Ptch1-/- cells. Development. 2014; 141: 3331-3339 [OpenAIRE] [PubMed] [DOI]

Lee, C.S., Buttitta, L., Fan, C.M.. Evidence that the WNT-inducible growth arrest-specific gene 1 encodes an antagonist of sonic hedgehog signaling in the somite. Proc. Natl. Acad. Sci. USA. 2001; 98: 11347-11352 [OpenAIRE] [PubMed] [DOI]

Yao, S., Lum, L., Beachy, P.. The ihog cell-surface proteins bind Hedgehog and mediate pathway activation. Cell. 2006; 125: 343-357 [OpenAIRE] [PubMed] [DOI]

Allen, B.L., Tenzen, T., McMahon, A.P.. The Hedgehog-binding proteins Gas1 and Cdo cooperate to positively regulate Shh signaling during mouse development. Genes Dev.. 2007; 21: 1244-1257 [OpenAIRE] [PubMed] [DOI]

Martinelli, D.C., Fan, C.M.. Gas1 extends the range of Hedgehog action by facilitating its signaling. Genes Dev.. 2007; 21: 1231-1243 [OpenAIRE] [PubMed] [DOI]

Tenzen, T., Allen, B.L., Cole, F., Kang, J.S., Krauss, R.S., McMahon, A.P.. The cell surface membrane proteins Cdo and Boc are components and targets of the Hedgehog signaling pathway and feedback network in mice. Dev. Cell. 2006; 10: 647-656 [OpenAIRE] [PubMed] [DOI]

Chuang, P.T., McMahon, A.P.. Vertebrate Hedgehog signalling modulated by induction of a Hedgehog-binding protein. Nature. 1999; 397: 617-621 [OpenAIRE] [PubMed] [DOI]

167 references, page 1 of 12
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publication . Article . 2016

Differential Cellular Responses to Hedgehog Signalling in Vertebrates—What is the Role of Competence?

Clemens Kiecker; Anthony Graham; Malcolm Logan;