publication . Other literature type . Article . Preprint . 2018

Cyclin G and the Polycomb Repressive complexes PRC1 and PR-DUB cooperate for developmental stability.

Delphine Dardalhon-Cuménal; Jérôme Deraze; Camille A. Dupont; Valérie Ribeiro; Anne Coléno-Costes; Juliette Pouch; Stéphane Le Crom; Hélène Thomassin; Vincent Debat; Neel B. Randsholt; ...
Open Access
  • Published: 11 Jul 2018
  • Publisher: Public Library of Science (PLoS)
  • Country: France
Abstract
In Drosophila, ubiquitous expression of a short Cyclin G isoform generates extreme developmental noise estimated by fluctuating asymmetry (FA), providing a model to tackle developmental stability. This transcriptional cyclin interacts with chromatin regulators of the Enhancer of Trithorax and Polycomb (ETP) and Polycomb families. This led us to investigate the importance of these interactions in developmental stability. Deregulation of Cyclin G highlights an organ intrinsic control of developmental noise, linked to the ETP-interacting domain, and enhanced by mutations in genes encoding members of the Polycomb Repressive complexes PRC1 and PR-DUB. Deep-sequencing...
Subjects
Medical Subject Headings: macromolecular substances
free text keywords: [SDV.BDD]Life Sciences [q-bio]/Development Biology, Research Article, Biology and Life Sciences, Cell Biology, Cell Processes, Cell Cycle and Cell Division, Cyclins, Developmental Biology, Morphogenesis, Imaginal Discs, Research and Analysis Methods, Experimental Organism Systems, Model Organisms, Drosophila Melanogaster, Animal Models, Organisms, Eukaryota, Animals, Invertebrates, Arthropoda, Insects, Drosophila, Genetics, Gene Expression, Biochemistry, Proteins, Protein Domains, Genomics, Animal Genomics, Invertebrate Genomics, DNA transcription, Life Cycles, Larvae, QH426-470, Genetics(clinical), Cancer Research, Ecology, Evolution, Behavior and Systematics, Molecular Biology
82 references, page 1 of 6

1. Palmer RA (1994) Fluctuating asymmetry analysis: a primer. In: Developmental Instability: Its Origins and Evolutionary Implications. Markow T. A. Netherlands, Kluwer Academic Publishers. pp. 335±364.

2. Nijhout F, Davidowitz G (2003) Developmental Perspectives on Phenotypic Variation, Canalization, and Fluctuating Asymmetry. In: Polak M, editors. Developmental instability, causes and consequences. New York: Oxford University Press. pp. 3±13.

3. Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annual review of physiology 61: 243±282. https://doi.org/10. 1146/annurev.physiol.61.1.243 PMID: 10099689

4. Queitsch C, Sangster TA, Lindquist S (2002) Hsp90 as a capacitor of phenotypic variation. Nature 417: 618±624. https://doi.org/10.1038/nature749 PMID: 12050657 [OpenAIRE]

5. Rutherford S, Knapp JR, Csermely P (2007) Hsp90 and developmental networks. Adv Exp Med Biol 594: 190±197. https://doi.org/10.1007/978-0-387-39975-1_16 PMID: 17205685 [OpenAIRE]

6. Debat V, Bloyer S, Faradji F, Gidaszewski N, Navarro N, et al (2011) Developmental Stability: A Major Role for Cyclin G in Drosophila melanogaster. PLoS Genet 7: e1002314. https://doi.org/10.1371/ journal.pgen.1002314 PMID: 21998598

7. Debat V, Peronnet F (2013) Asymmetric flies: The control of developmental noise in Drosophila. Fly (Austin) 7: 1±8. https://doi.org/10.4161/fly.23558 23519089 [OpenAIRE]

8. Van Valen L (1962) A study of fluctuating asymmetry. Evolution 16: 125±142. [OpenAIRE]

9. Palmer AR, Strobeck C (1992) Fluctuating asymmetry as a measure of developmental stability: Implications of non-normal distributions and power of statistical tests. Acta Zool. Fennica 191: 57±72. [OpenAIRE]

10. Dongen SV (2006) Fluctuating asymmetry and developmental instability in evolutionary biology: past, present and future. J Evol Biol 19: 1727±1743. https://doi.org/10.1111/j.1420-9101.2006.01175.x PMID: 17040371

11. Leamy L, Klingenberg C, Sherratt E, Wolf J, Cheverud J (2015) The Genetic Architecture of Fluctuating Asymmetry of Mandible Size and Shape in a Population of Mice: Another Look. Symmetry 7: 146±163. https://doi.org/10.3390/sym7010146 [OpenAIRE]

12. Rutherford SL, Lindquist S (1998) Hsp90 as a capacitor for morphological evolution. Nature 396: 336± 342. https://doi.org/10.1038/24550 PMID: 9845070

13. Milton CC, Huynh B, Batterham P, Rutherford SL, Hoffmann AA (2003) Quantitative trait symmetry independent of Hsp90 buffering: distinct modes of genetic canalization and developmental stability. Proc Natl Acad Sci U S A 100: 13396±13401. https://doi.org/10.1073/pnas.1835613100 PMID: 14595030

14. Debat V, Milton CC, Rutherford S, Klingenberg CP, Hoffmann AA (2006) Hsp90 and the quantitative variation of wing shape in Drosophila melanogaster. Evolution 60: 2529±2538.17263114 PMID: 17263114 [OpenAIRE]

15. Sangster TA, Salathia N, Undurraga S, Milo R, Schellenberg K, et al (2008) HSP90 affects the expression of genetic variation and developmental stability in quantitative traits. Proc Natl Acad Sci U S A 105: 2963±2968. https://doi.org/10.1073/pnas.0712200105 PMID: 18287065 [OpenAIRE]

82 references, page 1 of 6
Abstract
In Drosophila, ubiquitous expression of a short Cyclin G isoform generates extreme developmental noise estimated by fluctuating asymmetry (FA), providing a model to tackle developmental stability. This transcriptional cyclin interacts with chromatin regulators of the Enhancer of Trithorax and Polycomb (ETP) and Polycomb families. This led us to investigate the importance of these interactions in developmental stability. Deregulation of Cyclin G highlights an organ intrinsic control of developmental noise, linked to the ETP-interacting domain, and enhanced by mutations in genes encoding members of the Polycomb Repressive complexes PRC1 and PR-DUB. Deep-sequencing...
Subjects
Medical Subject Headings: macromolecular substances
free text keywords: [SDV.BDD]Life Sciences [q-bio]/Development Biology, Research Article, Biology and Life Sciences, Cell Biology, Cell Processes, Cell Cycle and Cell Division, Cyclins, Developmental Biology, Morphogenesis, Imaginal Discs, Research and Analysis Methods, Experimental Organism Systems, Model Organisms, Drosophila Melanogaster, Animal Models, Organisms, Eukaryota, Animals, Invertebrates, Arthropoda, Insects, Drosophila, Genetics, Gene Expression, Biochemistry, Proteins, Protein Domains, Genomics, Animal Genomics, Invertebrate Genomics, DNA transcription, Life Cycles, Larvae, QH426-470, Genetics(clinical), Cancer Research, Ecology, Evolution, Behavior and Systematics, Molecular Biology
82 references, page 1 of 6

1. Palmer RA (1994) Fluctuating asymmetry analysis: a primer. In: Developmental Instability: Its Origins and Evolutionary Implications. Markow T. A. Netherlands, Kluwer Academic Publishers. pp. 335±364.

2. Nijhout F, Davidowitz G (2003) Developmental Perspectives on Phenotypic Variation, Canalization, and Fluctuating Asymmetry. In: Polak M, editors. Developmental instability, causes and consequences. New York: Oxford University Press. pp. 3±13.

3. Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annual review of physiology 61: 243±282. https://doi.org/10. 1146/annurev.physiol.61.1.243 PMID: 10099689

4. Queitsch C, Sangster TA, Lindquist S (2002) Hsp90 as a capacitor of phenotypic variation. Nature 417: 618±624. https://doi.org/10.1038/nature749 PMID: 12050657 [OpenAIRE]

5. Rutherford S, Knapp JR, Csermely P (2007) Hsp90 and developmental networks. Adv Exp Med Biol 594: 190±197. https://doi.org/10.1007/978-0-387-39975-1_16 PMID: 17205685 [OpenAIRE]

6. Debat V, Bloyer S, Faradji F, Gidaszewski N, Navarro N, et al (2011) Developmental Stability: A Major Role for Cyclin G in Drosophila melanogaster. PLoS Genet 7: e1002314. https://doi.org/10.1371/ journal.pgen.1002314 PMID: 21998598

7. Debat V, Peronnet F (2013) Asymmetric flies: The control of developmental noise in Drosophila. Fly (Austin) 7: 1±8. https://doi.org/10.4161/fly.23558 23519089 [OpenAIRE]

8. Van Valen L (1962) A study of fluctuating asymmetry. Evolution 16: 125±142. [OpenAIRE]

9. Palmer AR, Strobeck C (1992) Fluctuating asymmetry as a measure of developmental stability: Implications of non-normal distributions and power of statistical tests. Acta Zool. Fennica 191: 57±72. [OpenAIRE]

10. Dongen SV (2006) Fluctuating asymmetry and developmental instability in evolutionary biology: past, present and future. J Evol Biol 19: 1727±1743. https://doi.org/10.1111/j.1420-9101.2006.01175.x PMID: 17040371

11. Leamy L, Klingenberg C, Sherratt E, Wolf J, Cheverud J (2015) The Genetic Architecture of Fluctuating Asymmetry of Mandible Size and Shape in a Population of Mice: Another Look. Symmetry 7: 146±163. https://doi.org/10.3390/sym7010146 [OpenAIRE]

12. Rutherford SL, Lindquist S (1998) Hsp90 as a capacitor for morphological evolution. Nature 396: 336± 342. https://doi.org/10.1038/24550 PMID: 9845070

13. Milton CC, Huynh B, Batterham P, Rutherford SL, Hoffmann AA (2003) Quantitative trait symmetry independent of Hsp90 buffering: distinct modes of genetic canalization and developmental stability. Proc Natl Acad Sci U S A 100: 13396±13401. https://doi.org/10.1073/pnas.1835613100 PMID: 14595030

14. Debat V, Milton CC, Rutherford S, Klingenberg CP, Hoffmann AA (2006) Hsp90 and the quantitative variation of wing shape in Drosophila melanogaster. Evolution 60: 2529±2538.17263114 PMID: 17263114 [OpenAIRE]

15. Sangster TA, Salathia N, Undurraga S, Milo R, Schellenberg K, et al (2008) HSP90 affects the expression of genetic variation and developmental stability in quantitative traits. Proc Natl Acad Sci U S A 105: 2963±2968. https://doi.org/10.1073/pnas.0712200105 PMID: 18287065 [OpenAIRE]

82 references, page 1 of 6
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